Monitoring of Stink Bugs in Blackberry and Life History of Euschistus Quadrator Rolston

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Monitoring of Stink Bugs in Blackberry and Life History of Euschistus Quadrator Rolston
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english
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Brennan, Sara Ann
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Degree:
Master's ( M.S.)
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University of Florida
Degree Disciplines:
Entomology and Nematology
Committee Chair:
Liburd, Oscar E
Committee Members:
Buss, Eileen A
Eger, Joseph E

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Subjects / Keywords:
blackberry -- euschistus -- ipm -- monitoring -- pheromones -- stinkbugs -- taxonomy
Entomology and Nematology -- Dissertations, Academic -- UF
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Entomology and Nematology thesis, M.S.
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Abstract:
Blackberry production in Florida has increased more than 100% within the last two decades and several insect pests, including stink bugs, have been feeding on this crop. Euschistus quadrator Rolston is a relatively new stink bug pest to Florida, and has spread throughout the state. The objectives for this study were to determine the stink bug species present in blackberry, to develop monitoring tools for stink bugs and to describe the life history and immature stages of E. quadrator. In a field survey, E. quadrator was the most abundant stink bug species, followed by E. servus Say, E. obscurus (Palisot de Beauvois), Thyanta custator (F.), Proxys punctulatus (Palisot de Beauvois) and Podisus maculiventris Say. In my monitoring studies, yellow pyramid traps were more effective than tube traps in catching stink bugs, with or without the addition of the Euschistus spp. pheromone. In a pheromone comparison experiment, there were no statistical differences between traps baited with a Trécé Pherocon Centrum lure, a Suterra Scenturion lure, and an unbaited trap. These results were supported by a Y-tube olfactometer assay where there were no differences between the lures and a control. Experiments to determine duration of immature stages of E. quadrator were conducted in the laboratory at 25 ± 0.5 degrees C and 50 ± 5% RH. I found that the duration of the six stadia of E. quadrator, egg through fifth instar, averaged 8.3, 6.1, 7.8, 6.8, 7.6 and 11.2 days, respectively. We found relatively low numbers of stink bugs in blackberries during the course of this study. However, under optimum conditions, stink bugs may warrant the development of pest management programs in blackberries to prevent them from reaching damaging levels.
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by Sara Ann Brennan.
Thesis:
Thesis (M.S.)--University of Florida, 2012.
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Adviser: Liburd, Oscar E.
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1 MONITORING OF STINK BUGS IN BLACKBERRY AND LIFE HISTORY OF EUSCHISTUS QUADRATOR ROLSTON By SARA ANN BRENNAN A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE UNIVERSITY OF FLORIDA 2012

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2 2012 Sara Brennan

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3 To my parents for their continued love and support

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4 ACKNOWLEDGMENTS I would especially like to thank my major professor, Dr. Oscar Liburd, for having fa ith in me, providing guidance and encouraging me throughout my studies. Thanks to other members of my graduate committee, Dr. Joe Eger and Dr. Eileen Buss, for their continued support and guidance. I deeply appreciate the assistance I received from the oth er members of the Small Fruit and Vegetable IPM laboratory in Gainesville, FL, as well as the employees of the Plant Science Research and Education Unit in Citra, FL. I would also like to thank Lyle Buss and Jane Medley for their assistance with photograph y and graphics. Thanks goes to all faculty and students of the Entomology and Nematology Department at the University of Florida, many of whom supported me in various ways throughout this journey. Finally, I cannot thank my parents enough for their moral s upport and encouragement throughout this process.

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5 TABLE OF CONTENTS page ACKNOWLEDGMENTS ................................ ................................ ................................ ............... 4 LIST OF TABLES ................................ ................................ ................................ ........................... 7 LIST OF FIGURES ................................ ................................ ................................ ......................... 8 ABSTRACT ................................ ................................ ................................ ................................ ..... 9 CHAPTER 1 INTRODUCTION ................................ ................................ ................................ .................. 11 2 LITERATURE REVIEW ................................ ................................ ................................ ....... 16 Stink Bugs ................................ ................................ ................................ ............................... 16 Euschistus servus ................................ ................................ ................................ ............. 17 Eus chistus quadrator ................................ ................................ ................................ ....... 18 Biology and Behavior ................................ ................................ ................................ ............. 19 Euschistus servus ................................ ................................ ................................ ............. 20 Euschistus quadrator ................................ ................................ ................................ ....... 20 Injury ................................ ................................ ................................ ................................ ....... 21 Monitoring and Management ................................ ................................ ................................ 23 Pheromones ................................ ................................ ................................ ..................... 23 Traps ................................ ................................ ................................ ................................ 24 Other Methods of Monitoring Stink Bug Populations ................................ .................... 25 Chemical Control ................................ ................................ ................................ ............. 26 Cultural Control ................................ ................................ ................................ ............... 27 Biological Control ................................ ................................ ................................ ........... 28 Organic Control ................................ ................................ ................................ ............... 29 Justification ................................ ................................ ................................ ............................. 30 Hypotheses ................................ ................................ ................................ .............................. 31 Specific Objectives ................................ ................................ ................................ ................. 31 3 STINK BUG SPECIES SURVEY IN BLACKBERRIES ................................ ..................... 32 Materials and Methods ................................ ................................ ................................ ........... 33 Results ................................ ................................ ................................ ................................ ..... 34 Discussion ................................ ................................ ................................ ............................... 35 4 MONITORING STINK BUGS IN BLACKBERRY ................................ ............................. 44 Materials and Methods ................................ ................................ ................................ ........... 46 Study Site ................................ ................................ ................................ ......................... 46

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6 Trap Comparison ................................ ................................ ................................ ............. 46 Pheromone Comparison ................................ ................................ ................................ .. 47 Laboratory study ................................ ................................ ................................ ...... 47 Field study ................................ ................................ ................................ ................ 48 Pheromone Concentration Comparison ................................ ................................ ........... 48 Data Analysis ................................ ................................ ................................ ................... 49 Results ................................ ................................ ................................ ................................ ..... 4 9 Trap Comparison ................................ ................................ ................................ ............. 49 Pheromone Comparison ................................ ................................ ................................ .. 50 Pheromone Concentration Comparison ................................ ................................ ........... 50 Discussion ................................ ................................ ................................ ............................... 51 5 LABORATORY REARING AND DESCRIPTIONS OF IMMATURE STAGES OF EUSCHISTUS QUADRATOR ................................ ................................ ................................ 63 Materials and Methods ................................ ................................ ................................ ........... 64 Laboratory Rearing ................................ ................................ ................................ .......... 64 Life History Study ................................ ................................ ................................ ........... 64 Descriptions of Immature Stages ................................ ................................ ..................... 65 Data Analysis ................................ ................................ ................................ ................... 65 Results ................................ ................................ ................................ ................................ ..... 65 Laboratory Rearing ................................ ................................ ................................ .......... 65 Immature Descriptions ................................ ................................ ................................ .... 66 F irst instar ................................ ................................ ................................ ................. 66 Second instar ................................ ................................ ................................ ............ 67 Third instar ................................ ................................ ................................ ............... 69 Fourth instar ................................ ................................ ................................ ............. 70 Fifth instar ................................ ................................ ................................ ................ 71 Discussion ................................ ................................ ................................ ............................... 72 6 GENERAL CONCLUSIONS ................................ ................................ ................................ 80 Species Survey in Blackberries ................................ ................................ .............................. 80 Monitoring in Blackberries ................................ ................................ ................................ ..... 81 Life History and Taxonomy o f E. quadrator ................................ ................................ .......... 81 LIST OF REFERENCES ................................ ................................ ................................ ............... 83 BIOGRAPHICAL SKETCH ................................ ................................ ................................ ......... 93

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7 LIST OF TABLES Table page 3 1 Species complex by sex in blackberries using the beating tray method ............................ 38 3 2 Numbers of each stink bug species collected by date ................................ ........................ 39 3 3 Numbers of stink bug species collected by blackberry variety (5/8/2010 6/19/2010) ...... 40 4 1 Species complex of stink bugs captured in trap comparison study ................................ ... 54 4 2 Chi square values for each treatment in Y tube assays (n=60) ................................ ......... 54 4 3 Species complex of stink bugs captured in pheromone comparis on study ........................ 55 4 4 Species complex of stink bugs captured in pheromone concentration comparison study ................................ ................................ ................................ ................................ ... 55 5 1 Duration (in days) of each immature stadium of E. quadrator under laboratory conditions ................................ ................................ ................................ ........................... 75 5 2 Head capsule (HC) length and width, and length of antennal segments (A#) of E. quadrator ................................ ................................ ....................... 76

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8 LIST OF FIGURES Figure page 1 1 Location and estimated number of blackberry farms in Florida in 2007 ........................... 15 3 1 Blackberry field layout in Citra, FL ................................ ................................ ................... 41 3 2 Species complex in blackberries using the beating tray method ................................ ....... 42 3 3 Total stink bug numbers correlated with mean percent fruit development in organic and conventional blackberry plots ................................ ................................ ..................... 43 4 1 Yellow pyramid trap with screen top ................................ ................................ ................. 56 4 2 Tube trap ................................ ................................ ................................ ............................ 57 4 3 Y tube olfactometer set up ................................ ................................ ................................ 58 4 4 Mean number of stink bugs captured in yellow pyramid traps (YP) or tube traps with (B) or without (UB) pheromone lures. Means followed by the same letter are not significantly different according to ANOVA ( F =4.93, df=5, P =0.0021). ......................... 59 4 5 Mean number of stink bugs captured in yellow pyramid traps baited with Trc or Suterra pheromone lures or without lures (UB). Means were not significantly different according to ANOVA ( F =1.80, df=5, P =0.1339). ................................ .............. 60 4 6 Mean number of stink bugs captured in yellow pyramid traps baited with one, two or three Trc lures or unbaited (UB). Means were not significantly different according to ANOVA ( F =2.23, df=5, P =0.0772). ................................ ................................ ............. 61 4 7 Percent stink bugs captured per species in field experiments (n=78) ................................ 62 5 1 Adult and nymph cage examples ................................ ................................ ....................... 77 5 2 Dorsal and ventral view of immature stages of Euschistus quadrator .............................. 78 5 3 Number of nymphs per instar that molted into each subsequent instar during the experiment ................................ ................................ ................................ .......................... 79

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9 Abstract of Dissertation Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science MONITORING OF STINK BUGS IN BLACKBERRY AND LIFE HISTORY OF EUSCHISTUS QUADRATOR ROLSTON By Sara Ann Brennan August 2012 Chair: Oscar Liburd Major: Entomology and Nematology Blackberry production in Florida has increased more than 100% within the last two decades and several in sect pests, including stink bugs, have been feeding on this crop. Euschistus quadrator Rolston is a relatively new stink bug pest to Florida, and has spread throughout the state. The objectives for this study were to determine the stink bug species present in blackberry, to develop monitoring tools for stink bugs and to describe the life history and immature stages of E. quadrator In a field survey, E. quadrator was the most abundant stink bug species, followed by E. servus Say, E. obscurus (Palisot de Bea uvois), Thyanta custator (F.), Proxys punctulatus (Palisot de Beauvois) and Podisus maculiventris Say. In my monitoring studies, yellow pyramid traps were more effective than tube traps in catching stink bugs, with or without the addition of the Euschistus spp. pheromone. In a pheromone comparison experiment, there were no statistical differences between traps baited with a Trc Pherocon Centrum lure, a Suterra Scenturion lure, and an unbaited trap. These results were supported by a Y tube olfactometer ass ay where there were no differences between the lures and a control.

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10 Experiments to determine duration of immature stages of E. quadrator were conducted in the laboratory at 25 0.5 C and 50 5% RH. I found that the duration of the six stadia of E. quadr ator egg through fifth instar, averaged 8.3, 6.1, 7.8, 6.8, 7.6 and 11.2 days, respectively. We found relatively low numbers of stink bugs in blackberries during the course of this study. However, under optimum conditions, stink bugs may warrant the devel opment of pest management programs in blackberries to prevent them from reaching damaging levels.

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11 CHAPTER 1 INTRODUCTION Commercial blackberry, Rubus ( Rubus ), production worldwide increased 45% from 1995 to 2005, producing 127,270 mt on 20,035 ha. During t he same time, U.S. production increased 34% to 28.884 mt on 4,818 ha, the highest production in the world in 2005 (Strik et al. 2007). Much of this increase in blackberry production is due to more efficient breeding of blackberry plants and an increase in consumer demand for more fruits and vegetables. In addition, blackberries are rich sources of antioxidants (polyphenols), which are believed to boost the (Moyer et al. 2002, Bowen Forbes et al. 2008). As the U.S. population becomes more health conscious, fruits high in antioxidants including blackberries are becoming increasingly popular. Blackberries were not a popular commercial crop until the 1990s due to the low quality and poor storage characteristics of the berries (Clark 1992). The development of thornless varieties has probably enabled blackberries to move from a primarily local crop to a nationwide retail crop. Although blackberries are mainly grown in the P acific Northwest, production in the southeastern U.S. is increasing. Georgia alone has tripled its production in the last 10 years (Strik et al. 2007). The USDA Plant Hardiness Zone Map shows that Georgia, Arkansas and Florida have overlapping plant hardin ess zones, classified by average extreme minimum temperature (USDA 2012). Georgia and Arkansas, which harvested 122 and 159 ha of blackberries in 2007 (USDA 2009b), respectively, have a humid subtropical climate (Kottek et al. 2006). Although northern Flor ida has a similar climate and plant hardiness zone, blackberry harvest in 2007 was limited to 40 ha, suggesting that there is room to increase production (USDA 2009b, USDA 2012).

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12 Blackberries have been grown on several small farms in Florida dating back to 1920 (USBC 1952). Blackberry harvest has slowly but steadily increased in the state and in the last two decades there has been >100% increase to 40 ha of blackberries harvested in the state of Florida (USDA 1994 2009a). Production in Florida occurs in 30 counties, with most farms concentrated in northern Florida (Anderson et al. 2011, Figure 1 1). Earlier ripening of blackberries in Florida may enable growers to meet a market window not currently being filled by other southern states. A similar case is see n in southern highbush other states (Williamson and Lyrene 2004). Recently, the University of Florida Institute of Food and Agriculture (IFAS), through the S mall Fruit and Vegetable IPM program, has established its first blackberry research site in Citra, Florida and had their first on in 2010. Blackberries and raspberries are members of the genus Rubus They have flowers with five petals, perennial roots and biennial shoots called canes (Crandall 1995). The canes do not produce flowers in the first year of growth, and are known as primocanes. In the second year, the canes produce fruit, and are known as floricanes (Jennings et al. 1 991). The flowers are produced in late spring or early summer, and fruits ripen within a couple of weeks. The canes die after they produce fruit, and new canes develop each year. T he plants must be pruned to remove floricanes after harvest to provide room for the new primocanes, which will fruit the following year. Blackberries typically grow best in temperate climates and commercial varieties have historically required low winter temperatures to stimulate flower bud development, limiting production to nort hern states (Jennings et al. 1991).

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13 In recent years, several lower chill and disease resistant blackberry cultivars have been developed, making them possible for commercial production in Florida (Jennings et al. 1991, Moore 1997, Clark 2005). The Universit y of Arkansas, in particular, has released several varieties of blackberries that exhibit favorable characteristics for commercial production in Florida. early, has good fruit quality, and fruits are of average size (Moore and Clark 1993). The gh yield a medium thorny, erect variety. Its fruit size is consistently large and its yields are similar to that of erect variety with a perform especially well in the South. This variety has a medium large fruit size and produces consistently high yields (Clark and Moore 2005). As blackberry production expands, pests and disease problems are expected to increase. Therefore, it is important to develop pest manage ment strategies to address potential threats. Flower thrips, Frankliniella spp., midges, Dasineura spp., and stink bugs (Pentatomidae) have been problematic in Georgia and Florida (Mizell 2007, O. E. Liburd, personal communication). These pests differ from the traditional northern pests of blackberries, which include aphids ( Aphis spp. ), Japanese beetles ( Popillia japonica Newman ) green June beetles ( Cotinis nitida (L.)) weevils ( Otiorhynchus spp.)) crown borers ( Pennisetia marginata (Harris) ), cane bore rs

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14 ( Oberea bimaculata (Olivier) Agrilus spp. ), leaf rollers ( Argyrotaenia franciscana ( Walsingham ), Choristoneura rosaceana (Harris) ) and mites ( Phyllocoptes gracilis ( Nalepa), Tetranychus urticae Koch) (Crandall 1995, Johnson and Lewis 2003). This new pe st complex may exist because of host shifts of insects onto the newer warm season varieties, expanded blackberry production into new areas, and the use of reduced risk pesticides targeted for other key pests. Nevertheless, integrated pest management tactic s are needed to address this new pest complex. In 2008 and 2009, large numbers of stink bugs were observed in blackberries and were suspected of injuring the fruit (O. E. Liburd, personal communication). The purpose of this research was to characterize the key stink bug species complex present in Florida blackberries. In addition, I compared and evaluated monitoring tools for key stink bugs [ Euschistus spp.] in blackberries and described the life history and immature stages of E. quadrator Rolston. My goal was to establish effective monitoring strategies that are environmentally friendly and economically practical for growers. There is little, if any research on stink bugs in blackberries, especially in the southeastern United States. With the new potential for stink bugs to cause injury to blackberries by feeding on the fruit and interfering with the quality of marketable yield, developing effective monitoring tools and understanding their biology will be important aspects of agricultural stink bug managemen t.

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15 Figure 1 1. Location and estimated number of blackberry farms in Florida in 2007

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16 CHAPTER 2 LITERATURE REVIEW Stink Bugs Stink bugs belong to the family Pentatomidae, which is the third largest family in the order Heteroptera, with over 4,000 known species (Schaefer and Panizzi 2000). Many phytophagous stink bugs are important pests, causing severe economic losses on a variety of plants (McPherson and McPherson 2000). Most stink bug species that are pests of crops belong to the subfamily Pentatominae (Schuh and Slater 1995). Stink bugs are highly polyphagous and mobile, often moving quickly through various crops and host plants. When crops are not fruiting, stink bugs may feed on wild hosts until crops become available (McPherson and McPherson 2000). This makes detection and management difficult. In addition, several stink bug species may form a species complex that attack various crops, increasing management difficulty (McPherson et al. 1979a). The most common stink bugs in this complex are the southe rn green stink bug, Nezara viridula (L.), the green stink bug, Chinavia hilaris (Say), and the brown stink bug, Euschistus servus (Say) (McPherson and McPherson 2000). The genus Euschistus not only contains E. servus but also other pest species in the con tinental United States such as Euschistus variolarius (Palisot de Beauvois), Euschistus tristigmus (Say), Euschistus ictericus (L.), Euschistus quadrator Rolston and Euschistus conspersus (Uhler). Euschistus quadrator and smaller species in the genus, such as E. obscurus their increasing pest status (Hopkins et al. 2005). Members of the genus Euschistus have been observed feeding on many cultivated crops includin g corn, Zea mays L., cotton, Gossypium hirsutum (L.), alfalfa, Medicago sativa L.,

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17 soybean, Glycine max L., and various fruits (McPherson and McPherson 2000). These species have migrated south, and increased in pest status in the southeastern United States in recent years. Most of the information gathered on the increasing pest status of Euschistus spp. is from Louisiana and Georgia. It is important to note that these states have a humid subtropical climate, with humid and hot summers and mild winters (Kott ek et al. 2006). Since Florida is characterized in the same climate zone, it is possible that these stink bugs will become more of a problem in Florida, as they have in other southeastern states. Euschistus servus The brown stink bug has two subspecies, E. s. euschistoides (Vollenhoven) and E. s. servus (Say). Euschistus servus servus occurs from Florida to California along the southern states, and E. s. euschistoides is in the northern half of the United States (McPherson 1982). The brown stink bug feeds p rimarily on soybean, cotton, corn and various fruits (McPherson and McPherson 2000, Schaefer and Panizzi 2000). Historically, the brown stink bug has been the most economically significant pest in this genus (McPherson and McPherson 2000). It is one of the most commonly collected stink bugs in many crops, along with the southern green stink bug and the green stink bug. Euschistus servus was recorded in Florida as early as 1886 in corn, although it was thought to be a predatory bug on the corn earworm, Helic overpa ( Heliothis ) armigera (Hbner) (Ashmead 1887). In 1908 and 1914, E. servus was commonly found all over Florida ( Van Duzee 1909, Barber 1914). pecan, cotton and rice ( Ashmead 1887, Hill 1938, Sprenkel 2008, Nuessly et al. 2010, Wright et al. 2011).

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18 Euschistus quadrator Euschistus quadrator is found across the southeastern U.S., and has been reported from Texas to Florida and north to Louisiana and Arkansas. It is most prominen t in Georgia soybean and cotton crops (McPherson et al. 1993). Euschistus quadrator was not described until 1974, much later than E. servus which was described in 1832 (Henry and Froeschner 1998). Euschistus quadrator was described from insects found in M exico, Texas and Louisiana (Rolston 1974), and was not found in Florida until 1992 (J. E. Eger, personal communication). It has since spread throughout the state and has become an agricultural pest of many fruit, vegetable and nut crops in the southeastern United States. Euschistus quadrator had previously been a secondary or tertiary pest, often found in very low numbers if at all. Euschistus quadrator has recently become a more prominent pest with the introduction of crops such as Bt cotton, which does no t control stink bugs, and reduced application of broad spectrum insecticides. The first record of E. quadrator on cotton was in 1998 in southern Georgia (Bundy and McPherson 2000b). It was listed as a pest of concern for the southeastern United States in 2 007 (Brambila 2007). In addition to Bt cotton, reduced use of broad spectrum insecticides may have led to a resurgence of stink bugs as agricultural pests (Greene et al. 2001). Euschistus quadrator has been noted in several different crops, sometimes as pr ominent as E. servus (Hopkins et al. 2010). It has recently been a key pest listed in soybean and corn (Ruberson et al. 2009, Hopkins et al. 2010, Tillman 2010b, Olson et al. 2011). This suggests that the pest species complex may be changing, with E. quadr ator increasing in pest status. Within 10 years of its discovery in cotton, E. quadrator was listed as a common pest and increasingly abundant in southern Georgia (Ruberson et al. 2009, Tillman et al. 2009a).

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19 Biology and Behavior Stink bugs in southeastern crops are characterized by having a shield shaped body, ranging in size from approximately 9 to 15 mm in length, depending on the species (McPherson 1982, Schaefer and Panizzi 2000). They have a segmented beak arising from the front of the head, five segm ented antennae, three segmented tarsi, membranous hind wings, and forewings (hemelytra) that are leathery basally and membranous distally (McPherson and McPherson 2000). The scutellum is usually triangle shaped. They garner their common name from their abi lity to secrete a foul smelling liquid from glands on their thorax when threatened. These scent glands occur dorsally on nymphs and adults (Schuh and Slater 1995, McPherson and McPherson 2000). Mating begins in the spring and eggs are laid in clusters with tight rows. Eggs are cylinder Euschistus spp. range in length from approximately 0.88 to 1.15 mm, and diameter from approximately 0.71 to 1.03 mm (Bundy and McPherson 20 00a). Egg clusters are usually geometrically or irregularly shaped. The incubation period for eggs can be anywhere from 3 days to 3 weeks depending on the species and environmental conditions. There are five nymphal instars. First instars remain on or near the eggs in clusters, and disperse to find water and food sources around the time of the first molt ( McPherson and McPherson 2000 ). Development from egg to adult ranges from 23 to 58 days, depending on the species and environmental conditions (Schaefer an d Panizzi 2000). Adults commonly overwinter beneath leaf litter or mulch. Overwintering adults become active in spring, which is usually when the first generation appears. Overwintering adults typically colonize spring vegetables, mullein, Verbascum thapsu s (L.), white clover and other wild hosts ( McPherson and McPherson 2000 ). Euschistus servus and E. quadrator are both bivoltine in the southern United States (McPherson 1982, Munyaneza and McPherson 1994, Herbert and Toews 2011). Most species in the genus Euschistus have very similar life histories.

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20 Euschistus servus Euschistus servus is most often between 11 and 15 mm long (McPherson 1982). It usually overwinters under crop residues and weeds, especially common mullein and winter wheat, Triticum aestivum L (Rolston and Kendrick 1961, Buntin and Greene 2004,). These hosts may provide an environment for E. servus to build up and subsequently move into important cash crops. The egg masses of E. servus are semi translucent and light yellow, and range between 2 8 to 55 eggs per cluster. Bundy and McPherson (2000a) found a maximum of 35 eggs per cluster for E. servus (Esselbaugh 1946, Woodside 1946). Earlier, Rolston and Kendrick (1961) recorded that E. servus eggs have an incubation period ranging from 3 to 14 da ys, with an average of 5.5 days, while Munyaneza and McPherson (1994) found a range of 5 to 7 days with an average of 5.8 days. Euschistus servus nymphs complete their development in approximately 23 to 63 days, averaging around 33 days according to Rolsto n and Kendrick (1961) and 44.3 days according to Munyaneza and McPherson (1994) at 23 C. Euschistus quadrator Adults are shield shaped and light to dark brown in color. They are smaller than many other members of the genus, generally around 9 mm in length and approximately 5 mm wide across the abdomen (Esquivel et al. 2009). Euschistus quadrator lacks dark spots in the membranous area of the hemelytra, a characteristic present in other species of Euschistus commonly found in southeastern crops (Esquivel et al. 2009). The eggs of E. quadrator are semi translucent and light yellow, and become more red as the eggs mature (S. A. Brennan, personal observation). The micropylar processes (fan like projections around the top of the egg) are longest in this species compared with other Euschistus

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21 spp. (Bundy and McPherson 2000a). Bundy and McPherson (2000a) found a maximum of 25 eggs per cluster in their research. Little is known about E. quadrator nymphs. Injury Stink bugs have piercing sucking mouthparts and most f eed primarily on fruits and seeds, causing injury to various fruits and vegetables, and resulting in significant quality and yield loss (Schaefer and Panizzi 2000, Panizzi 1997). Stink bugs pierce plant tissues with their stylets, causing physical injury t hat resembles a pinprick. They also inject digestive enzymes to aid in injury in the form of discolored spots on the fruit or deformed areas, rendering the fruit unma rketable. Stink bugs can also transmit various microorganisms, which cause plant diseases, such as yeast spot disease in soybeans (Daugherty 1967). A stylet sheath is often left behind at the feeding site (Bowling 1979, 1980). Due to the relatively new pes t status of stink bugs in blackberries, very little to no research has been conducted in this area. Morrill (1910) first reported an observation of E. servus feeding on Rubus sp. Stink bugs feed between or on the drupelets of bramble berries and this can r esult in collapsed or leaky drupelets that render the fruit unmarketable for commercial growers (D. G. Pfeiffer, personal communication). Furthermore, stink bug feeding can alter the taste of the fruit, which can negatively affect its marketability (S. A. Brennan, personal observation). For instance, when a bug is disturbed, it releases its defensive chemicals onto the fruit, which causes the fruit to have a distinctive taste. This is especially important in mechanically harvested berries where stink bugs a re continuously disturbed with the mechanical harvester (DeFrancesco et al. 2002). Stink bugs in other crops Stink bugs were first reported on cotton in the early 20 th century (Cassidy and Barber 1939). They have historically been a secondary pest of cott on, but are increasing in pest status (Greene et al. 2001). This is most likely due to the transition from

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22 growing conventional cotton dominated by broad spectrum insecticide applications to transgenic cotton for control of the lepidopteran complex (McPher son and McPherson 2000). The first record of E. quadrator in cotton was in 1998 in southern Georgia (Bundy and McPherson 2000b). By 2004 and later in 2007, E. quadrator was listed as a common pest in cotton in southernmost Georgia (Ruberson et al. 2009, Ti llman et al. 2009a). Stink bugs, including E. servus occur in most regions where soybean is grown in the United States (Turnipseed and Kogan 1976). Members of the genus Euschistus commonly found in soybean include E. servus, E. obscurus E. quadrator E. tristigmus and E. ictericus (Todd 1982, Orr et al. 1986). In the mid 1970s, E. quadrator was rare in soybean in Louisiana (McPherson 1982). Observations by Orr et al. (1986), however, in the early 1980s show a significant increase in numbers of E. quadrat or also in Louisiana. In Georgia, McPherson et al. (1993) found low numbers of E. quadrator in soybean during a five year study in the late 1980s. However, increasing reports of E. quadrator in other crops in southern Georgia may lead to an increased pest status of E. quadrator in southern grown soybean (Ruberson et al. 2009). Cotton, soybean and other crops are often grown in close proximity. Olson et al. (2011) determined that E. servus in southwestern Georgia strongly preferred soybean over Bt cotton, no n Bt cotton, and peanut. This supports the earlier work of Bundy and McPherson (2000b), who found higher numbers of E. servus in soybean than in cotton. Similarly, Herbert and Toews (2011) and Olson et al. (2011) found soybean to be a more suitable host fo r reproduction of E. servus than cotton, peanut and corn. Since some varieties of soybean have a long bloom and fruit set period, they may support populations of stink bugs for long periods of time, allowing them to move into other near by crops (Toews and Shurley 2009).

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23 Stink bug pest status has also been increasing in corn. Townsend and Sedlacek (1986) attributed some of this increase into cultural control changes in the production of corn and adoption of Bt corn as an alternative strategy for management of lepidopteran pests as opposed to the use of broad spectrum insecticides. Tillman (2010b) found all developmental stages of E. quadrator and E. servus in Georgia corn fields, suggesting that corn is a reproductive host for these stink bug species (Tillma n 2010b). Monitoring and Management Stink bugs are mobile, polyphagous pests, making monitoring and management difficult (McPherson and McPherson 2000). There are only a few commercial methods that have been used for monitoring stink bugs in blackberry (De Francesco et al. 2002, Johnson and Lewis 2003). Most monitoring information comes from crops such as cotton, pecan, peaches and soybean. Since stink bugs are polyphagous, monitoring methods may differ between crops. Visual searches, ground cloths, blacklig ht traps, fruit injury, beating and sweep net samples have historically been used to determine stink bug infestation levels (Todd and Herzog 1980). Many of these methods are labor intensive and can be biased against catching nymphs or adults. Sweep netting for example is inefficient in some crops, such as corn and cotton, and can catch more late instar nymphs and adults (Toews and Shurley 2009). Pheromones Several species of stink bugs produce pheromones that attract other stink bugs and aid in the aggrega tion of stink bugs in the field (Todd and Herzog 1980, Krupke et al. 2001). It is believed that these male produced pheromones are aggregation pheromones, as both sexes are attracted to the pheromones in field studies (Aldrich et al. 1991, Millar et al. 20 02, Leskey and Hogmire 2005). Pheromones can be used to improve monitoring efficiency in the field.

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24 Aldrich et al. (1991) trapped volatiles from male and female Euschistus spp. using gas chromatography, they found a sex specific component, methyl (2 E ,4 Z ) d ecadienoate, produced by males. This pheromone attracts males, females and nymphs of several Euschistus spp. and is a major component for E. servus E. politus (Uhler), E. ictericus E. conspersus and E. tristigmus (Aldrich et al. 1991). Although direct st udies of volatile secretions of E. quadrator have not been conducted, this species is caught in traps baited with the Euschistus spp. pheromone (Tillman and Cottrell 2012, S. A. Brennan, personal observation). Traps Mizell and Tedders (1995) modified a pyr amid trap initially developed by Tedders and Wood (1994) to monitor for the pecan weevil, Curculio caryae (Horn). The modified pyramid trap is used extensively in pecan and peach orchards. These pyramid traps are most effective when painted with industrial safety yellow paint as opposed to other colors, indicating that the color yellow may be an attractive visual stimulus for stink bugs (Mizell and Tedders 1995, Leskey and Hogmire 2005). Yellow pyramid traps have increased attraction when paired with the Eu schistus spp. pheromone, methyl (2 E ,4 Z ) decadienoate, offering a more convenient and efficient method of sampling compared to visual searches, sweep netting or insecticidal sprays (Aldrich et al. 1991, Cottrell 2001, Leskey and Hogmire 2005). This trap has detected stink bug migration into peach and blackberry, with and without the addition of the pheromone (Mizell 2008b). However, the rate of escape from these traps depends on the cage used on top of the trap. Cottrell (2001) found the rate of escape decre ases when using an insecticidal ear tag inside the trap, which did not decrease attraction of Euschistus spp. to the trap in pecan orchards. Hogmire and Leskey (2006) were able to significantly reduce escape of Euschistus spp. by reducing the cone opening inside the trap, and increasing jar size, with or without an insecticidal ear tag in apple and peach orchards.

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25 Tube traps made from clear plastic tubes with wire mesh cones on the ends have been used in several studies with varying results, and are still c ommercially available for monitoring stink bugs. Krupke et al. (2001) caught very few stink bugs using two variations of the tube trap in mullein, while Aldrich et al. (1991) used these traps to test their Euschistus spp. pheromone in weedy areas or blackb erry patches, and caught a large numbers of stink bugs. Other Methods of Monitoring Stink Bug Populations A relatively new method of detection involves monitoring for the vibrational signals of stink bugs using accelerometers. Many types of insects use pla nts as a type of transmission channel for vibrational songs, which can be used for courtship, rivalry songs and female acceptance songs (Michelsen et al. 1982). Stink bugs communicate at short range by generating vibrational signals through a plant using a tymbal organ located underneath the elytra. These vibrations are transmitted and detected through the legs. These signals have been characterized for C. hilaris and N. viridula (Millar et al. 2002). Lampson et al. (2010) found four different songs for mal es and two different songs for females in cotton, the same number of songs previously reported for E. conspersus and E. heros (F.). These songs are species specific, allowing for discrimination between species for monitoring. Although this method is new, t here seems to be promise in providing information on stink bugs in the field. However, additional costs of labor and materials may render this method impractical. Regardless of the sampling method, it should be noted that stink bugs have a pronounced edge effect in most field crops. In cotton, stink bug damage and colonization are associated mostly within crop edges (Tillman et al. 2009b, Toews and Shurley 2009). Edge effects have also been noted in corn, peanut and wheat ( Reay Jones 2010, Tillman 2010b, 20 11a). Thus, to improve sampling efficiency and reduce costs, sampling should occur on the edges of fields, depending on the crop.

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26 Chemical Control Stink bugs can be tolerant to some insecticides, and the use of insecticides can kill beneficial insects, cau se harm to the environment and repeated use may cause insecticide resistance (Crandall 1995). Historically, recommendations for stink bug control included broad spectrum pesticides such as dichlorodiphenyltrichloroethane (DDT), parathion, lindane and dield rin (Borden et. al. 1952) Organophosphates, such as methyl parathion, dicrotophos and acephate, are used extensively to control stink bug pests in soybean and cotton (McPherson et al. 1979b, Chyen et al. 1992, Willrich et al. 2003, Tillman and Mullinix 2 004, Snodgrass et al. 2005). Methyl parathion and dicrotophos are listed as Category 1 insecticides by the Environmental Protection Agency (EPA). This is the most toxic out of four categories of insecticides (EPA 1991, Chyen et al. 1992). These insecticide s have demonstrated negative effects on parasitoids and predators of stink bugs, such as Trissolcus basalis (Wollaston), Telenomus podisi Ashmead and Podisus maculiventris (Say) (Orr et al. 1989, Sudarsono et al. 1992, Tillman and Mullinix 2004). Alternati ves to methyl parathion are pyrethroids (Chyen et al. 1992, Greene et al. 2001). Pyrethroids including bifenthrin (Category 2), cyhalothrin ( Category 2), cyfluthrin ( Category 3), and cypermethrin ( Category 3) have also shown some efficacy against stink bugs. Generally, Euschistus spp. are less susceptible to these insecticides than other stink bug species (Willrich et al. 2003, S nodgrass et al. 2005). Cyfluthrin is more toxic to beneficial insects than E. servus (Tillman and Mullinix 2004). Willrich et al. (2003) and Snodgrass et al. (2005) found that brown stink bugs were more susceptible to bifenthrin compared with other pyrethr oids that are effective against other stink bug species. To achieve significant bug mortality us ing other cyhalothrin and cypermethrin

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27 had the least effect on E. servus cyhalothrin exhibited similar effects on E. quadrator (Willrich et al. 2003). Intra species differences in s usceptibility to insecticides have been shown for Euschistus spp., N. viridula and C. hilaris (Snodgrass et al. 2005). Variation within life stages of a species has also been demonstrated to show varying levels of susceptibility. Generally, fewer insectici des are effective against Euschistus spp. than other pest species. In addition, late instar nymphs of Euschistus spp. can be more susceptible to different insecticides than adults of the same species (Willrich et al. 2003). Methyl parathion, even at a high er rate, does not provide adequate control of E. servus fifth instars (McPherson et al. 1979b). This reiterates the fact that effective and accurate monitoring tools must be implemented to ensure that plot management tactics including insecticides target t he proper species and life stages. Cultural Control Trap crops Trap crops are used to attract and keep pest species away from the cash crop, prevent them from entering the cash crop mechanically or to enhance natural enemy populations (Hokkanen 1991). Tra p crops are planted at a specific space and time, depending on the pest species and cash crop. Utilizing a trap cropping system can reduce insecticide applications to the main crop, preserve more natural enemies, and combat other issues such as pest insect icide resistance (Hokkanen 1991). In some cases, the trap crop can be treated with insecticides to further reduce pest pressure. Trap crops are especially efficient considering that stink bugs prefer field borders, as well as their tendency to aggregate as nymphs (McPherson and McPherson 2000). In many instances, stink bug infestations are closely related to the phenology of the cash crop. This can be exploited by planting trap crops at particular times to attract stink bugs away from the cash crop (Hokkane n 1991, McPherson and McPherson 2000). Early maturing soybean varieties have

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28 shown promise as a trap crop for conventional soybean (McPherson et al. 2001). Stink bugs typically colonize these early maturing varieties before moving into conventional soybean as the early varieties senesce. This temporal difference would enable the grower to minimize insecticide treatments in the conventional soybean, and predict stink bug infestations based on crop phenology (Smith et al. 2009). Many different species of plan ts are recommended for trap cropping of stink bugs, depending on the cash crop. Triticale [ Triticale hexaploide Lart .], sorghum [ Sorghum bicolor (L.)], millet [ Pennisetum glaucum (L.)], buckwheat [ Fagopyrum sagittatum Gilib], sunflower [ Helianthus annus L. ], soybean, field peas [ Phaseolus vulgaris L.], okra [ Abelmoschus esculentum Moench] and others have been evaluated as potential trap crops for stink bugs (Bundy and McPherson 2000b, Mizell 2008a, Olson et al. 2011, Tillman 2011b). Biological Control Paras itoids Biological control methods do exist, as most Euschistus spp. are susceptible to parasitoids and predators (McPherson and McPherson 2000). Stink bugs are attacked by several different parasitoids and predators at both the immature and adult stages. Telenomus podisi is a common egg parasitoid of E. servus along with Trissolcus euschisti Ashmead T. basalis T. brochymenae (Ashmead) T. thyantae Ashmead, Ooencyrtus spp. and Trissolcus edessae Fouts (Yeargan 1979, Orr et al. 1986, Koppel et al. 2009, Ti llman 2010a ). In addition to egg parasitoids, several parasitoids attack adult Euschistus spp., with Gymnoclytia immaculata (Macquart), Cylindromyia euchenor (Walker), and Euthera tentatrix Loew attacking E. quadrator and Trichopoda pennipes (F.), Gymnocl ytia occidua (Walker), C. euchenor E. tentatrix and Gymnosoma fuliginosum Robineau Desvoidy attacking E. servus (Eger and Ables 1981, McPherson et al. 1982). Ruberson et al. (2009) found the first record in

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29 the Americas of the braconid wasp, Aridelus ruf otestaceus Tobias parasitizing E. servus in Georgia soybean. Tillman et al. (2010) discovered that a common tachinid parasitoid of E. servus, Cylindromyia sp., was attracted to the aggregation pheromone, methyl ( 2 E ,4 Z ) decadienoate, used for monitoring Eus chistus spp. in the field. Other parasitoids that use this pheromone as a host finding kairomone are Gymnosoma spp. and Euthera spp. (Aldrich et al. 1991). Many chewing and sucking predators attack stink bug eggs. These include minute pirate bugs ( Orius sp p.), the cotton fleahopper, ( Pseudatomoscelis seriatus (Reuter)) a plant bug ( Spanagonicus sp.), the spined soldier bug, ( Podisus maculiventris ) the big eyed bugs ( Geocoris uliginosus (Say) and G. punctipes (Say)) and several species of ants and lady bee tles ( Yeargan 1979, Ruberson et al. 2009, Tillman 2010a, 2011b). Stink bugs also feed on their own eggs in the field and laboratory (Ruberson et al. 2009, S. A. Brennan, personal observation). Ruberson et al. (2009) also discovered the first record of fung al infection of E. servus They were unable to identify the fungus because it was not sporulating, but determined that it belonged the fungal order Entomophthorales, a group of entomopathogenic fungi. Organic Control Relatively few products are effective f or stink bug control in organic crops. With a organic produce, only a few insecticides have been labeled for organic pest control. Three organic insecticides that hav e been used for stink bugs are azadirachtin (Neem), pyrethrins (PyGanic) and spinosad (Entrust). Azadirachtin is derived from the neem tree, Azadirachta indica (A. Juss), and exhibits feeding deterrency and growth disruptive properties (Mordue and Blackwel l 1993). It is effective against other insects, such as Japanese beetles and locusts as a feeding deterrent (Butterworth

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30 and Morgan 1971, Ladd et al. 1978) Kamminga et al. (2009) found that E. servus adults were susceptible to azadirachtin when mixed with spinosad or pyrethrins. Azadirachtin treated tomatoes had fewer stylet sheaths than untreated tomatoes, however azadirachtin had no effect on stink bugs in a filter paper repellency test (Kamminga et al. 2009). Pyrethrins are derived from plants in the fa mily Compositae, such as Chrysanthemum cinerariifolium (Trev.), and can cause rapid knockdown and eventual death of insects by effecting nerve function (Casida 1980). Pyrethrins were used in the early 1800s to control body lice and many other household and agricultural pests (Casida 1980). Kamminga et al. (2009) found that E. servus adults and nymphs were only susceptible to pyrethrins when mixed with spinosad. They were effective, however, in repelling stink bugs when applied to tomatoes and filter paper ( Kamminga et al. 2009). Spinosad is from a class of insecticides, spinosyns, which are derived from a soil microorganism, Saccharopolyspora spinosa ( Mertz and Yao ) (Sparks et al. 1998). Spinosad acts as a contact poison and is effective against many differe nt pests, including thrips and lepidopteran pests, and is less toxic to beneficial predators (Boyd and Boethel 1998, Sparks et al. 1998, Kamminga et al. 2009). Euschistus servus adults are susceptible to spinosad, alone or tank mixed with azadirachtin or p yrethrins, but nymphs are not affected (Kamminga et al. 2009). However, spinosad treated tomatoes had no effect on E. servus and insects were attracted to it in filter paper repellency tests (Kamminga et al. 2009). Justification Stink bugs have the potenti al to cause injury to blackberry as well as other fruit crops by feeding on the fruit and reducing the marketable yield. They are highly polyphagous and several techniques, including use of sweep nets, fruit injury, in situ counts and pheromone baited trap s, have been used to monitor stink bugs. For instance, pheromone baited traps painted with

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31 industrial safety yellow enamel paint have been used successfully to monitor brown stink bugs, E. servus the dusky stink bug, E, tristigmus and the green stink bug C. hilaris (Leskey and Hogmire 1995). Developing an effective monitoring protocol may reduce reliance on routine pesticide applications and give growers time to respond to increasing populations. Correct identification is important to select the most appr opriate pest management tools. Pest management tools, including pesticides, are only effective against certain species (Flint and Gouveia 2001). To facilitate correct identification of E. quadrator detailed descriptions of the immatures were reported here in. Adults were not described since they were described by Rolston (1974). Hypotheses H 0 : Stink bugs are present in blackberry H A : Stink bugs are not present in blackberry H 0 : The yellow pyramid trap will be more effective than the tube trap for monito ring stink bugs in blackberry H A : There are no differences between the yellow pyramid trap and tube trap for monitoring stink bugs in blackberry H 0 : The addition of pheromone lures will increase trap captures of stink bugs. H A : Pheromone lures do not in crease trap captures for stink bugs. Specific Objectives 1. To identify key stink bug species in blackberry. 2. To describe the immature stages of Euschistus quadrator 3. To evaluate traps and pheromone lures in the subsequent categories for monitoring stink bug s pecies: a) trap comparison in blackberry field test, b) pheromone lure comparison in blackberry field tests and laboratory bioassays.

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32 CHAPTER 3 STINK BUG SPECIES SU RVEY IN BLACKBERRIES Since blackberries are a relatively new crop for the southeast, most of the recommended pest management information applies to the northwestern United States where blackberries have been an important crop for decades. However, many pest species present in other areas affect blackberries in the southeast. Thrips, spider mites, stink bugs and beetles have been listed as pests of concern for Florida, and these pests are also present in the northwest (Ellis et al. 1991, Mizell 2007, O. E. Liburd, personal communication ). Euschistus spp., the southern green stink bug, Nezara viridu la (L.) and the green stink bug, Chinavia hilaris (Say), have been reported as pests of blackberries (Johnson and Lewis 2003, Anonymous 2008, Mizell 2008a ), and the brown stink bug, Euschistus servus (Say), causes injury to other Rubus spp. crops (Maxey 20 11) With a southern shift in blackberry production, it is likely that stink bugs will become more of an issue in blackberry crops. Historically, the most commonly collected stink bugs in many crops are the brown stink bug, E. servus the southern green st ink bug and the green stink bug (McPherson and McPherson 2000). In recent years, E. quadrator Rolston and other minor species in the genus are increasing 2005). Members of the genus Euschistus have been found in corn, cotton, rice, soybean, pecan and peach in Florida ( Ashmead 1887, Hill 1938, Temerak and Whitcomb 1984, Mizell 2008b, Sprenkel 2008, Nuessly et al. 2010, Wright et al. 2011). In 2008 and 2009, large numbers of stink bugs (several species) were observed in blackberries in Citra, Florida (O. E. Liburd, personal communication). With the changing pest complex and potential future increases in blackberry production in the southeast, it is necessary to iden tify and survey any new pest species, including stink bugs, which may pose a threat to increasing production. Here, we used a

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33 knockdown technique to monitor the species complex in blackberries. This technique involves placing a collecting device on the gro und at the base of the plant. The plant is then shaken vigorously until the pest species is dislodged from its host and falls into the collecting device. Insects are then placed into a collecting jar and later identified to species. The specific objective for this study was to identify stink bug species present in blackberry. Materials and Methods Research was conducted at the University of Florida, Plant Science Research and Education Unit in Citra, Florida, and at the Small Fruit and Vegetable IPM laborat ory in Gainesville. The experimental site in Citra consists of two 0.12 ha sites, each composed of six (Figure 3 1). Each row is approximately 38 m long with 30 blac kberry plants, and rows are spaced approximately 4.5 m apart. Half of the site is managed as a traditional conventional site and the other is managed as an organic site. Blackberry plants were approximately 3 years old and 1.5 meters tall. Each site was wa tered using a hard line with in line emitters as needed, not exceeding 2500 3000 gallons/acre/day. Drip irrigation was placed in middle of each row. The organic plot received half the amount of water as the conventional plot. Organic plots were covered wit h DeWitt landscaping tarp [DeWitt Company, Sikeston, MO]. Hydrosource water gathering crystals [ Castle International Resources, Sedona, Arizona ] in various sizes (medium and standard) were added to the soil in the organic plots for water retention (Figure 3 1). After fruiting, floricanes were pruned to allow room for the primocanes. Blackberries were grown on a moving arm shift trellis (Stiles 1999). Both conventional and organic plots were sprayed with copper sulfate as a fungicide. Conventional plots also Research Triangle Park,

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34 NC AgraQuest, Inc., Davis, CA] With respect to nutrition, conventional plots were fertilized with 10 10 10 and the o rganic plots were fertilized with Nature Safe 10 2 8 [Nature Safe Cold Spring, KY]. Weed control in MO], whereas weeds were hand pulled from the organic plot. Sampl ing was conducted on four randomly chosen blackberry plants of each variety in both blackberry plots. A harvest tray (~ 1 x 0.6 m) [Wal Mart, Gainesville, FL] was placed on the ground at the base of the blackberry bush. Bushes were shaken vigorously 3 4 ti mes over the tray and the cover of the tray replaced immediately. Sampling occurred once every 2 wk for 8 wk. All stink bug species that fell into the tray were collected. In 2010, stink bugs were sampled from May 8 th to June 19 th when bushes were more tha n 50% fruiting. Stink bugs from each sample were transferred to collecting jars and labeled by date, sample and variety. All jars were brought back to the Small Fruit and Vegetable IPM laboratory at the University of Florida in Gainesville, FL. All stink b ugs were counted, mounted, pinned and identified to species using a key to the Florida families of Pentatomidae developed by Dr. J. Eger. Data Analysis. All information is presented as raw data (total counts) due to low numbers of stink bugs found in the f ield. Results A total of 54 stink bugs were collected in the blackberry plot throughout the sampling period. Table 3 1 represents the species collected including E. quadrator which was the most abundant, followed by E. servus E. obscurus (Palisot de Beau vois), Thyanta custator (F.), Proxys punctulatus (Palisot de Beauvois) and the spined soldier bug, Podisus maculiventris Say (Figure 3 2). Both males and females of most species were found in the field (Table 3 1). Only

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35 adults were collected, which may mea n that blackberries are not a reproductive host for these stink bugs. Other insects collected included ants (Hymenoptera: Formicidae), spiders (Arachnida: Araneae: Salticidae ; Arachnida: Araneae: Oxyopidae), grasshoppers (Insecta: Orthoptera: Acrididae), p lant bugs (Insecta: Hemiptera: Miridae), katydids (Insecta: Orthoptera: Tettigoniidae) leaffooted bugs (Insecta: Hemiptera: Coreidae), lady beetles (Insecta: Coleoptera: Coccinellidae) and flower beetles, Euphoria sepulcralis (F.) (Coleoptera: Scarabaeida e). Discussion The first visual sighting of stink bugs was of E. servus on 28 April 2010 in the organic plot. The organic plot began fruiting after the conventional, but fruit became riper faster in the organic plot, which may have been more attractive to stink bugs. Although overall stink bug numbers were low, there is a general correlation between the number of stink bugs found on each sampling date with the amount of ripe fruit in each plot. As the percent of ripe fruit increased in both the organic and conventional plots, the number of stink bugs also increased (Figure 3 3). During sampling, most stink bugs were found on the third sampling date (6/5/2010), when most berries were ripe (Table 3 2). An approximately equal number of stink bugs were found in the organic plot (28) and the conventional plot (26) (Table 3 3). The Chickasaw variety produced the most stink bugs across both the conventional and organic plots. This variety ripens approximately 1 wk later than Kiowa and Natchez varieties. Several new pest records for blackberries were found. This is the first known record of E. quadrator E. obscurus T. custator P. punctulatus and P. maculiventris in blackberry. Little, if any, information has been published in journals on the stink bug complex in b lackberries. The limited information available is on websites, which state that green stink bugs, southern green stink bugs and brown stink bugs are most prominent.

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36 The majority of stink bug information in Florida, especially for Euschistus spp., is from t he early 20 th century. A review of the literature shows that, historically, the pest status of stink bugs in Florida is debatable. The most commonly mentioned stink bugs in the state are N. viridula E. servus and E. ictericus (L.). Nezara viridula is comm only found in rice, soybean, faba bean and various weeds in southern Florida (Buschman and Whitcomb 1980, Temerak and Whitcomb 1984, Jones and Cherry 1986, Nuessly et al. 2004, Cherry and Wilson 2011). Euschistus servus is usually seen in pecans, soybean, elderberry and goldenrods in Florida (Hill 1938, Frost 1979, Fontes et al. 1994). Euschistus ictericus is found in rice and faba bean (Temerak and Whitcomb 1984, Jones and Cherry 1986,Nuessly et al. 2004, Cherry and Wilson 2011). There is no doubt that the se pests occur in other Florida crops, but literature with this information was not found. Other documented occurrences of Euschistus spp. in Florida include E. obscurus in elderberry and goldenrod, and E. quadrator in faba bean (Frost 1979, Fontes et al. 1994, Nuessly et al. 2004). Given this information, we expected to find mostly green stink bugs and E. servus in field trials. When using any monitoring device, care should be taken in identifying the stink bug species present. Euschistus servus is relativ ely easy to identify versus other Euschistus spp., but E. ictericus E. tristigmus (Say) and P. maculiventris look very similar, and the smaller brown stink bugs of the are easily confused. Predatory stink bugs, such as the spined soldier bug, may be mistaken as pests. Podisus maculiventris is a beneficial predatory stink bug that mostly feeds on lepidopteran and coleopteran larvae, but has been shown to feed on phytophagous stink bugs (McPherson et al. 1980, McPherson and M cPherson 2000). Predatory stink bugs can be differentiated from phytophagous stink bugs most easily by the mouthparts. Predatory stink bugs have a short and thick first rostral segment, which is free

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37 from the body. Phytophagous stink bugs have a slender fi rst rostral segment that appears to attach at the anterior tip of the head ventrally (Mizell 2008b). The yellow pyramid traps capture both predatory and pest species using the Euschistus spp. pheromone (Mizell 2008a). Of the other insects found, several be neficials were collected including ants (Formicidae), spiders (Salticidae and Oxyopidae), and lady beetles (Coccinellidae). Other pest species included grasshoppers (Acrididae), plant bugs (Miridae), katydids (Tettigoniidae), leaffooted bugs (Coreidae) and flower beetles, Euphoria sepulcralis (F.). This species of beetle is common in Florida and known for feeding on flowers and ripe fruit ( Frost 1979, Turner and Liburd 2007). Overall, blackberries in Florida seem to have a different stink bug complex than that of other production areas. While we found several Euschistus spp. that are commonly mentioned in other areas, we did not find either the green stink bug or the southern green stink bug. It is also interesting to note that so many different Euschistus spp. were found on the blackberries at the same time, and that E. quadrator was the dominant species.

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38 Table 3 1. Species complex by sex in blackberries using the beating tray method Species Male Female Unknown Total E. quadrator 11 10 21 E. servus 7 5 12 E. obscurus 5 4 9 T. custator 3 3 6 P. punctulatus 0 2 1 3 P. maculiventris 0 3 3 Total 54

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39 Table 3 2. Numbers of each stink bug species collected by date Date E. quadrator E. servus E. obscurus P. maculiventris T. custator P. punctu latus Total 5/8/2010 3 0 1 2 0 0 6 5/22/2010 4 2 3 1 1 0 11 6/5/2010 9 4 5 0 3 2 23 6/19/2010 5 6 0 0 2 1 14 Total 21 12 9 3 6 3 54

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40 Table 3 3. Numbers of stink bug species collected by blackberry variety (5/8/2010 6/19/2010) Blackberry # of Stink Bugs Variety Organic Conventional Kiowa 3 7 Ouachita 7 3 Arapaho 3 1 Choctaw 3 1 Chickasaw 10 8 Natchez 2 6 Total 28 26

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41 Figure 3 1. Blackberry field layout in Citra, FL

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42 Figure 3 2. Species comp lex in blackberries using the beating tray method

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43 Figure 3 3. Total stink bug numbers correlated with mean percent fruit development in organic and conventional blackberry plots

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44 CHAPTER 4 MONITORING STINK BUG S IN BLACKBERRY B lackberry production in the southeastern United States is increasing. Georgia has tripled its production in the last 10 years and harvested 122 ha of blackberries in 2007 (Strik et al. 2007, USDA 2009) Similarly, blackberry production has increased fivefo ld in Florida (O. E. Liburd, personal communication). Traditionally, blackberry production in Florida only involved small backyard operations and small (<0.3) ha u pick operations. Now, growers are experimenting with larger acreage (3 5 ha). Currently tota l production in Florida is estimated between 5 75 ha and increasing. Florida, along with much of the southeast, has a humid subtropical climate, which is likely to support good blackberry yield (Kottek et al. 2006). Earlier ripening of blackberries in Flor ida may enable growers to meet a market window not currently being filled by other southern states. In recent years, several blackberry cultivars have been developed to be more tolerant to the climatic conditions of the southern United Sates, making these states a candidate for commercial blackberry production (Jennings et al. 1991, Moore 1997). Pest and disease problems are expected to increase as blackberry production expands into these states. Recent sightings of large numbers of stink bugs and other het their roles in blackberry production in these non traditional states. It is possible that stink bugs will become more of a problem in blackberries as they have in other southeastern crops. Very little research has been conducted on stink bugs in blackberries. Stink bugs cause feeding injury in blackberries in the form of collapsed or leaky drupelets that render the fruit unmarketable for growers (D. G. Pfeiffer, personal communication). Moreover, stink bug feeding can alter the taste of the fruit, which can also negatively affect its marketability (S. A. Brennan, personal observation).

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45 Stink bugs are highly mobile and polyphagous pests, which makes monitoring difficult (McPherson and McPherson 200 0). Visual searches, ground cloths, blacklight traps, fruit injury, beating and sweep net samples have typically been used to determine stink bug infestation levels (Todd and Herzog 1980). Many of these methods are labor intensive and can be biased against catching nymphs or adults (Toews and Shurley 2009). The addition of pheromones can be used to improve monitoring efficiency in the field. Aldrich et al. (1991) trapped volatiles from male and female Euschistus spp., and using gas chromatography, found tha t the major component produced by males is methyl (2 E ,4 Z ) decadienoate. This pheromone attracts males, females and nymphs of several Euschistus spp. (Aldrich et al. 1991). Euschistus quadrator Rolston was also caught in yellow pyramid traps baited with the Euschistus spp. pheromone (Tillman and Cottrell 2012, S. A. Brennan, personal observation). A commonly used trap for stink bugs, the yellow pyramid trap, was developed by Mizell and Tedders (1995). These pyramid traps are most effective when painted with industrial safety yellow as opposed to other colors (Leskey and Hogmire 2005, Mizell and Tedders 1995). Yellow pyramid traps have been shown to increase attraction of stink bugs when paired with the Euschistus spp. pheromone [methyl (2 E ,4 Z ) decadienoate], offering a more convenient and efficient method of sampling for stink bugs compared to other methods (Aldrich et al. 1991, Cottrell 2001, Leskey and Hogmire 2005). This trap has detected stink bug migration into blackberry, with and without the addition of the pheromone (Mizell 2008a). Tube traps made from clear plastic tubes with wire mesh cones on the ends have been used in several studies with varying results, and are commercially available for monitoring stink bugs. Krupke et al. (2001) caught very few stink bugs using two variations of the tube trap. However,

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46 Aldrich et al. (1991) used these traps to test their Euschistus spp. pheromone and caught large numbers of stink bugs. With the increase in blackberry production in and around Florida, as well as t he apparent elevation in pest status of stink bugs, determining an effective monitoring tool for selected stink bug species is essential for growers. The specific objectives of this study were: 1. To compare commercial traps for monitoring stink bugs in black berries 2. To compare pheromone lures for captures of stink bug species in a Y tube assay and field deployment experiments. Materials and Methods Study Site Research was conducted at the University of Florida, Plant Science Research and Education Unit in Citr a, Florida, and at the Small Fruit and Vegetable IPM laboratory in Gainesville, Florida. Trap Comparison Two different types of commercially available stink bug traps, 1) Yellow Pyramid trap [R. Mizell, Quincy, FL] and 2) Trc tube trap [Great Lakes IPM, Vestaburg, MI], were compared with and without pheromone lures. Pyramid traps were constructed as recommended by Dr. Russell F. Mizell (Mizell 2008a). Both the Trc Pherocon Centrum lure [Trc Inc., Adair, OK] and Suterra Scenturion lure [Suterra Corpora te, Bend, OR] were used in each baited trap since information on the lure that performs the best was unavailable. Four treatments were evaluated as follows: 1) Pyramid trap baited, 2) Pyramid trap unbaited, 3) Trc trap baited, and 4) Trc trap unbaited. The experiment was a completely randomized block design with three replicates. Blackberry bushes were approximately 3 years

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47 The yellow pyramid trap was placed just east of the row approximately 0.5 m from the bushes (Figure 4 1). The Trc tube trap was hung from the trellis inside the bush approximately 1 m from the ground (Figure 4 2). Traps were spaced a minimum of 15 m apart and were blocked by variety (row). Traps were placed on the first, third and fifth rows. Trap contents were emptied into collecting jars and rotated weekly for three weeks. All stink bug species were brought back to the Small Fruit and Vegetable IPM laboratory at the Univ ersity of Florida to be counted, mounted, pinned and identified. Pheromone Comparison Laboratory study A bioassay was conducted in a glass Y tube olfactometer [Chemglass Life Sciences, Vineland, NJ]. Humidified airflow was maintained at 1,000 ml/min using a 2 channel air delivery system, with two glass flowmeters, an acrylic chassis, two charcoal filters, and two gas bubblers [Analytical Research Systems, Gainesville, FL]. The glass Y tube (150 mm main tube, 80 mm arms, 35 mm internal diameter, 40/35 joints ) was held at a 30 angle inside a cardboard box (44 30 23 cm) on a piece of foam core set at a 5% incline (Figure 4 3). Preliminary studies indicated that E. quadrator responded better at a 5% incline as opposed to a horizontal surface. Foam core and interior of box were white. A hole was cut into the side of the box at the end of the Y tube so that pheromones did not collect and pool inside the box. Two mason jars, located outside of the box, were modified to house the lures during the assay (Figure 4 3). Holes were drilled into the lids, and valves were secured to the lids that were connected to the plastic tubing attached to the filtration system. Two commercially available aggregation pheromone lures for monitoring Euschistus spp., 1) Trc Pherocon Centrum lure and 2) Suterra Scenturion lure, were compared in the Y tube bioassay. Treatments were compared as follows: 1) Trc Pherocon Centrum lure against a blank

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48 control, 2) Suterra Scenturion lure against a blank control, and 3) Trc Pherocon Centr um lure versus Suterra Scenturion lure. Stink bugs were placed in the Y tube base and allowed to acclimate for 3 min before attaching the Y tube arms and airflow. Stink bugs were evaluated to determine their preference, and the time it took them to make a decision was recorded. A choice was considered made after the insect remained in one of the arms for 1 min. Stink bugs were considered unresponsive after staying in the Y tube for 15 min without making a choice. Adult stink bugs > 1 month old were used in the assay. A total of 20 responding stink bugs per treatment were evaluated, with the jars being rotated after 10 stink bugs to prevent positional bias. Field study Two different aggregation pheromone lures marketed commercially for stink bug monitoring we re evaluated, 1) Trc Pherocon Centrum lure and 2) Suterra Scenturion lure. Yellow pyramid traps were used because my preliminary trap comparison research indicated that these traps performed better than tube traps. Three treatments were compared as follo ws: 1) Trc Pherocon Centrum lure, 2) Suterra Scenturion lure and 3) unbaited trap. Experimental design was a completely randomized block with four replicates. Traps were placed just east of the row approximately 0.5 m from the bushes. Traps were spaced a minimum of 15 m apart and were blocked by variety (row). Traps were placed in the first, third, fifth and sixth rows. Trap contents were emptied into collecting jars and traps were rotated weekly. All stink bug species were brought back to the Small Fruit and Vegetable IPM laboratory at the University of Florida to be counted, mounted, pinned and identified. Pheromone Concentration Comparison The Trc Pherocon Centrum lure was evaluated in three different concentrations (treatments) as follows: 1) one lur e, 2) two lures and 3) three lures. These treatments were

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49 compared to an unbaited control. The Trc Pherocon Centrum lure was used because it performed numerically better than the Suterra Scenturion lure in previous field experiments. All treatments were used with the yellow pyramid trap. Experimental design was a completely randomized block with three replicates. Traps were placed just east of the row approximately 0.5 m from the bushes. Traps were spaced a minimum of 15 meters apart and were blocked by v ariety (row). Traps were placed in the first, third and fifth rows. Traps were sampled once per week for 4 weeks. All stink bug species were brought back to the Small Fruit and Vegetable IPM laboratory at the University of Florida to be counted, mounted, p inned and identified. Data Analysis Field experiments were arranged in a randomized complete block design. Resulting data were analyzed using analysis of variance (ANOVA) and differences among means were determined using a least significant difference (LSD ) mean separation test (0.05) (PROC GLM, SAS Institute 2008). The Y tube assay data were analyzed using a chi square analysis with an expected probability of 0.5. A t test was used to determine any significant differences between sexes of Euschistus spp. c aught in traps (0.05) (PROC TTEST, SAS Institute 2008). Results Trap Comparison There was a significant difference between trap types, with the yellow pyramid trap catching more stink bugs than the tube trap (Figure 4 4; F =4.93, df=5, P =0.0021). However, t here were no significant differences between a baited and unbaited pyramid or tube trap. Both males and females were caught in the traps, but there were no statistical differences between sexes (t=0.49, P =0.6526).

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50 The species recorded for this experiment, in order of abundance, consisted of Euschistus servus (Say) being the most common, followed by E. quadrator Podisus maculiventris Say, E. obscurus (Palisot de Beauvois), Euschistus ictericus (L) and Thyanta custator (F.) (Table 4 1). Pheromone Comparison In the Y tube assays, there were no statistical differences between any of the treatments (Table 4 2). In the Trc lure versus a blank control, 12 stink bugs chose the lure and 8 chose the blank control ( 2 = 0.8, df=1, P =0.3711). In the Suterra lure versu s a blank control, 10 stink bugs each chose the lure or the blank control ( 2 = 0.0, df=1, P =1.00). In the Trc lure versus the Suterra lure, 13 stink bugs chose the Trc lure and 7 chose the Suterra lure ( 2 = 1.8, df=1, P =0.1797). There were a total of 1 2 non responders, distributed fairly evenly across all treatments. Similar to my Y tube assays, no significant differences were found in the field tests that compared pheromone baited pyramid traps with and unbaited pyramid traps (Figure 4 5; F =1.80, df=5, P =0.1339). Numerically, traps baited with the Trc lure caught more stink bugs (n=10), but not enough to be significantly more effective than the Suterra lure or unbaited traps. The unbaited traps captured five stink bugs, and the Suterra lure caught sev en. The species composition for this experiment consisted of E. servus being the most common, followed by T. custator E. quadrator and E. ictericus (Table 4 3). Both males and females were caught in the traps, but there were no statistical differences bet ween sexes (t=0.18, P =0.8648). Pheromone Concentration Comparison There were no significant differences between traps baited with any pheromone load rates and unbaited traps (Figure 4 6; F =2.23, df=5, P =0.0772). The species composition for this experiment consisted of E. servus being the most common, followed by E. quadrator T. custator E. ictericus and P. maculiventris (Table 4 4).

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51 Both males and females were caught in the traps, but there were no statistical differences between sexes (t= 0.88, P =0.4309). Discussion In the trap comparison experiment, no stink bugs were caught in the tube traps. This is similar to the observations of Krupke et al. (2001), where very low numbers of stink bugs were captured when comparing two different sizes of tube trap. How ever, Aldrich et al. (1991) caught a significant number of stink bugs in the genus Euschistus using the tube trap in a deciduous forest. This indicates that tube traps may not be effective in blackberry crops but may have potential uses in other crops. Thi s may be due to the fact that stink bugs may rely more on the visual cues of the pyramid trap, or that they may tend to remain on or near berry clusters and not in the foliage of the plant. The pyramid traps were effective in catching stink bugs, either wi th or without the addition of the Euschistus spp. pheromone. Overall, stink bug numbers were relatively low, so there were no statistical differences between a baited and an unbaited trap. Most studies using the pyramid trap find that the addition of the E uschistus spp. pheromone increases the efficacy of the trap (Leskey and Hogmire 2005). In the pheromone comparison experiment, there were no statistical differences between the Trc Pherocon Centrum lure, the Suterra Scenturion lure and an unbaited trap. Again, stink bug numbers were low, which may account for the observed non significant differences and the obvious similarities in effectiveness. However, these results were supported by the Y tube olfactometer assay where there were no statistical differen ces between the lures and a control, although higher numerical values were recorded with the Trc lure when using E. quadrator One of the reasons why the Y tube assay did not show differences might be related to the fact that stink bugs can be overwhelme d by the presence of a large amount of pheromones. This has also been hypothesized by Krupke et al. (2001). The Y tube used in this experiment was

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52 modified with mason jars to possibly counteract this effect. The composition of these commercial lures was un known since this was proprietary information that the companies would not disclose. Since there were no statistical differences between lures, both in the field and in the Y tube bioassay, there are a number of factors that may merit further study. These f actors include the ratio of pheromone components of the lure, the previous experience of the insects, food or mate availability and the release rates of the lures. Species found in field experiments include E. quadrator E. servus E. obscurus T. custato r E. ictericus and P. maculiventris (Figure 4.7). Only adult stink bugs were caught in monitoring traps, and both males and females were caught. Since no statistical differences between sexes were found, it can be determined that this trap attracts both m ales and females. Stink bugs appear to colonize blackberry when berries are mid ripe to fully ripe. In the trap comparison experiment, a total of 35 total stink bugs were found, with the majority found in traps located in the Kiowa variety. Kiowa ripens ea rlier than most varieties in early June, and fruiting extends for six weeks (Moore and Clark 1996). The peak in stink bug numbers occurred during the week of 5/5/2010, when berries were mid ripe. In the pheromone comparison experiment, most stink bugs were found during the week of 5/26/2010 in Kiowa and Natchez when berries were beginning to ripen. Natchez also ripens early in June, and fruiting extends for four weeks (Clark and Moore 2008). In the pheromone concentration experiment, most stink bugs were fo und in Kiowa in the week of 7/7/2010 when berries were ripe. Proxys punctulatus (Palisot de Beauvois) was not caught in traps during field studies, but was found in the species survey experiment (Chapter 5). This stink bug has been found previously in the pyramid trap (Mizell 2008a). It has been suspected of being predaceous but is also known to feed on plants and weeds, such as cotton, Gossypium hirsutum (L.), and zigzag

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53 spiderwort, Tradescantia subaspera Ker (Vangeison and McPherson 1975, Gomez and Mizell 2009). These stink bugs are not thought to cause significant economic damage (Schaefer and Panizzi 2000). With the pyramid trap, several different tops can be used with the yellow pyramid base. Although rate of escape was not calculated during the experim ents, observations between sampling dates indicated that stink bugs are able to escape when using the screen top. Cottrell (2001) found a high rate of escape when using 2.8 L jar tops and that Euschistus spp. have a high rate of escape within 24 hours of b eing put in the trap when using a jar top. Later, Hogmire and Leskey (2006) found that by decreasing the jar opening and increasing the jar size, the rate of escape can be reduced. The plans followed for these experiments include a 2.5 inch opening on the screen top, which may have accounted for a few escapes. If using a screen top, the addition of an insecticidal ear tag may help prevent escape. Based on findings from other studies, it may be more effective to use a jar top on the trap as opposed to a scre en top, although this may be more costly for growers. Overall, the yellow pyramid trap was more effective than the tube trap for monitoring stink bugs in blackberry. The pheromone lures were no more effective than an unbaited trap, however this may be a re sult of low stink bug numbers in the field. In both field studies and the Y tube assay, the Trc Pherocon Centrum lure performed better numerically than the Suterra Scenturion lure or an unbaited trap but there were no significant differences. The screen top may have a higher rate of escape than other tops, but the addition of an insecticidal ear tag may counteract this effect. This research may provide information for growers who are considering the purchase of available lures as to which lure is more pra ctical and whether a lure is needed for their field setting.

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54 Table 4 1. Species complex of stink bugs captured in trap comparison study Species Male Female Total E. quadrator 5 1 6 E. servus 5 10 15 E. obscurus 1 3 4 T. custator 1 0 1 E. ictericus 1 3 4 P. maculiventris 0 5 5 Total 35 Table 4 2. Chi square values for each treatment in Y tube assays (n=60) Treatment 2 P Trc vs. Control 0.8 0.3711 Suterra vs. Control 0 1 Suterra vs. Trc 1.8 0.1797

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55 Table 4 3. Species complex of stink bugs captured in pheromone comparison study Species Male Female Unknown Total E. quadrator 2 1 3 E. servus 2 6 1 9 E. obscu rus 0 0 0 T. custator 3 3 2 8 P. punctulatus 0 0 0 E. ictericus 2 0 2 E. tristigmus 0 0 0 Total 22 Table 4 4. Species complex of stink bugs captured in pheromone concentration comparison study Species Male Female Total E. quadrator 2 3 5 E. servus 8 2 10 T. custator 1 3 4 E. ictericus 1 0 1 P. maculiventris 0 1 1 Total 21

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56 Figure 4 1. Yellow pyramid trap with screen top (Photo credit by: Sara Brennan)

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57 Figure 4 2. Tube trap (Photo credit by: Sara Brennan)

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58 Figure 4 3. Y tube olfactometer set up. A ) jar 1, B ) jar 2, C ) air filtration system, D ) modified cardboard box, E ) aeration hole, F ) foam board

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59 Figure 4 4. Mean number of stink bugs captured in yellow pyramid traps (YP) or tube traps with (B) or without (UB) pheromone lures. Means followed by the same letter are not significantly different according to ANOVA ( F =4.93, df=5, P =0.0021).

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60 Figure 4 5. Mean number of stink bugs captured in yellow pyramid traps b aited with Trc or Suterra pheromone lures or without lures (UB). Means were not significantly different according to ANOVA ( F =1.80, df=5, P =0.1339).

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61 Figure 4 6. Mean number of stink bugs captured in yellow pyramid traps bait ed with one, two or three Trc lures or unbaited (UB). Means were not significantly different according to ANOVA ( F =2.23, df=5, P =0.0772).

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62 Figure 4 7. Percent stink bugs captured per species in field experiments (n=78)

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63 CHAPT ER 5 LABORATORY REARING A ND DESCRIPTIONS OF I MMATURE STAGES OF EUSCHISTUS QUADRATOR Adults of Euschistus quadrator Rolston were not described until 1974, and its pest status remained very low until the mid 1990s. Adults were described from insects found in Mexico, Texas and Louisiana (Rolston 1974), but nymphal stages have not been described. Descriptions of immature stages of occasional or secondary pests are important especially if pest status is likely to change in the future. Euschistus quadrator is abu ndant in Georgia soybean and cotton (McPherson et al. 1993). However, the first record of E. quadrator in Florida occurred in 1992, and it has since spread throughout the state (J. E. Eger, personal communication). It was listed as a pest of concern in the southeastern United States in 2007 (Brambila 2007). Euschistus quadrator has been noted in several different crops, where it is as abundant as Euschistus servus (Say) (Hopkins et al. 2010). It was recently listed as a key pest in cotton, soybean and corn (Ruberson et al. 2009, Hopkins et al. 2010, Tillman 2010b, Olson et al. 2011). This suggests that the pest species complex may be changing, with E. quadrator increasing in pest status. Tillman (2010b) found all developmental stages of E. quadrator in Georg ia corn fields. Since E. quadrator caused similar cotton boll damage as E. servus in cage studies, this may indicate that E. quadrator has the potential to cause as much injury as E. servus to crops (Hopkins et al. 2005). Since E. quadrator is often found in same habitats as E. servus there is potential for confusion when trying to identify the stink bug species present. Differences in insecticide susceptibility have been shown for E. servus and E. quadrator as well as intra species differences ( McPherson et al. 1979b, Willrich et al. 2003, Snodgrass et al. 2005). With the potential for damage by stink bugs, including the correct

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64 identification is the key for developing appropriate IPM tools for managing these pests. Since adults have already been described (Rolston 1974), describing the immature stages of E. quadrator to allow identification of this species would be of significant help to growers and extension personnel who are trying to identify the stink bug species pres ent in their crops. The specific objective of this study was t o establish rearing protocol to: a) determine the duration of immature life stages of Euschistus quadrator b) describe the immature stages of Euschistus quadrator Materials and Methods Laborat ory Rearing A laboratory colony was established and maintained for several months from wild caught E. quadrator adults from a variety of host plants. Adults were caged in groups of 8 10 males and females. Cages (15 15 18 cm) were made from plastic food storage containers [Target, Minneapolis, MN ] with holes in the lids ( ~ 4 5 cm) and sides covered with 0.3 mm mesh screens for aeration (Figure 5 1). Each cage contained a 59.2 mL Solo souffl cup with lid [Solo Cup Company, Lake Forest, IL] with a cott on roll [1 cm diameter, cut to 5 cm length, Richmond Dental, Charlotte, NC] inserted into a hole cut into the lid for a water source (Figure 5 1). Adults were reared on organic green beans, roma beans and cherry tomatoes. A strip of cheesecloth was taped t o the inside of the cage for oviposition. Cages were kept in a rearing incubator on a 16L:8D photoperiod at 25 0.5 C and 50 5% relative humidity (RH). Life History Study The life history study began on 1/31/2012. All egg clusters were removed daily, th e number of eggs laid per cluster was counted, then egg clusters were placed into individual 5.5 cm Petri dishes for 7 days. Although egg clusters were laid all over each cage, only clusters laid on the cheesecloth were used. Clusters were checked daily be tween 1400 and 1500 hours for any

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65 molting activity. Nymphs were counted by instar per egg cluster. When nymphs reached the second instar, they were transferred to a 473.18 ml clear plastic container with lid [Solo Cup Company, Lake Forest, IL] with filter paper in the bottom to provide extra room (Figure 5 1). Nymphs were fed organic green beans only, which were changed every 2 3 days as needed. The number of eggs that hatched were calculated to determine % survival. The stadium for each instar in days and incubation period for eggs in days were also determined. Descriptions of Immature Stages Ten live nymphs of each instar were photographed and measured using Auto Montage Pro software [version 5.02, Syncroscopy, Frederick, MD] and a Leica MZ12.5 stereomicro scope. Length was measured from the tip of the tylus to the tip of the abdomen, and width was measured at the second abdominal segment on first through third instars, and just below wing pads on fourth and fifth instars. Head capsule width was measured acr oss the compound eyes, and head capsule length was measured from the tip of the tylus to the back of the head. Data Analysis Means and standard errors were reported for the number of days required for development from egg to 1 st instar, as well as other im mature stages (2 nd 3 rd 4 th and 5 th instars). Cumulative mean age and the number of days required to complete each stadium were also calculated. Data were analyzed using Microsoft Excel [Microsoft Office Professional Plus 2010, Redmond, WA ] where appropr iate. Results Laboratory Rearing In this study, eggs were laid in clusters of 2 to 39, averaging 15.01 eggs per cluster (n=54). A total of 812 eggs were laid on cheesecloth over the 7 day period. 754 of these eggs were viable, and 425 hatched. The incubati on period averaged 8.3 days (Table 5 1). The first through

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66 fifth stadia averaged 6.1, 7.8, 6.8, 7.6 and 11.2 days, respectively. The total developmental time from egg to adult averaged 47.7 days (Table 5 1). Of the insects that molted into adults, 51% were male (137 insects) and 49% were female (133 insects), placing the sex ratio at approximately 1:1. Immature Descriptions First instar Figure 5 2A Length 1.06 0.01 mm; width 1.00 0.01 mm. Form ovoid to nearly circular, convex dorsally, usually longer t han broad, greatest width at abdominal segments 2 3. No or few visible punctures on dark brown areas. Head declivent, narrowly rounded anteriorly, anterolateral margins slightly sinuate, posterior margin broadly convex; yellowish brown to brown dorsally, w ith vertex often more yellow medially and tylus yellowish brown; tylus surpassing juga; apical half of head sparsely setose, white line extending from each eye posteromedially and disappearing beneath pronotum. Eyes red. Antennae 4 segmented; segments 1 2 brown to red; segment 3 yellowish red to brown; segment 4 longest, fusiform, reddish brown to brown, incisures lighter, distinct constrictions at junctures of 2 3 and 3 4, ratio of segment length approximately 2:3:3:7; segments 2 and 3 sparsely setose, set ae moderately dense on 4 th segment. Ventral surface of head yellowish brown. Rostrum 4 segmented; yellowish brown basally, becoming darker brown distally. Thoracic nota brown, yellowish brown medially, yellow mediolongitudinal line extending from anterior margin of pronotum to posterior margin of metanotum; lateral margins entire and slightly explanate. Thoracic nota with posterior margins broadly arcuate. Thoracic pleura dark brown, pro and mesopleura fused to respective nota; metapleuron separated from m etanotal plate by membranous area. Spiracles on posterior margins of pro and mesopleura. Sterna yellowish red, concolorous with ventral surface of abdomen. Coxae and trochanters yellowish

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67 brown, coxae with brown spot on lateral surface; femora brownish re d to red; tibiae reddish brown to yellow, legs sparsely setose; tarsi, tarsal claws and pulvilli yellowish; tarsi 2 segmented and darker at apex. Dorsum of abdomen yellow with red markings, markings variable in density. Yellowish brown to brown medial and lateral plates present. Eight medial plates present; plates 1 and 2 on corresponding abdominal segments, small and transversely linear, plate 3 traversing segments 3 and 4, transversely linear and slightly constricted medially; plate 4 traversing segments 4 and 5, subrectangular with irregular margins, slightly more narrow than and 3 4 times medial length of plate 3, yellowish red anchor shaped marking present; plate 5 traversing segments 5 and 6, subtrapezoidal with irregular margins, same width or slightl y more narrow than plate 4, narrower posteriorly, 4 5 times medial length of plate 3, yellowish anchor shaped marking present; plate 6 located on segment 7, approximately same width as posterior third of plate 5, variable in shape, often split or partially split medially; plate 7 located on segment 8, often similar in size and shape to plate 6, but not split medially, plate 9 fused to lateral plates on segment 9. Paired ostioles of scent glands located near intersegmental suture laterally on plates 2, 3, 4. Nine lateral plates present, triangular in shape dorsally, rounded to subquadrate ventrally, plate 1 smaller, plates 2 7 largest and similar in size, plate 7 occasionally slightly smaller, plate 8 decreasing in size posteriorly, plate 9 fused to medial pl ate 8. Spiracles located on segments 2 7, each located in dark brown macule. Single trichobothrium located posteromesad to each spiracle on segments 3 7, small dark macule usually present at base of trichobothria. Second instar Figure 5 2B Length 1.90 0 .05 mm; width 1.27 0.02 mm. Form broadly pyriform; dorsum of head and thorax with numerous punctate brown spots; ventral punctures minute or absent.

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68 Similar to previous instar except as follows, head slightly declivent, lateral margins of juga slightly s inuate; yellowish red dorsally with dark brown band posteriorly, oval brown spot medial to each eye, vertex concolorous with remainder of dorsal surface. Antennal segment 1 dark brown to black proximally and reddish yellow distally, segment 2 reddish, segm ent 3 white, incisures reddish brown, segment 4 brown, setae increasing in density distally; ratio of segment lengths approximately 4:7:6:10. Ventral surface of head dark brown except for ventral surface of juga and white markings around base of antennae. First two rostral segments paler than last two segments. Thoracic nota yellowish white; lateral margins explanate, dentate, occasionally with sparse brown spots. Posterior margins of mesonotum angulate; intersegmental lines between segments darker brown fr om either side of midline to at least half way between lateral margin and midline of body; pronotum with black marking within cicatrices, mesonotum with two pairs, metanotum with one pair, of irregular brown markings. Pleura whitish yellow, with irregular brown bands and scattered punctures. Coxae white to brown, usually with darker margins and brown central spot; trochanters white; femora white basally, proximal one third to one half brown and slightly setose; tibiae reddish brown to brown, often reddish b asally, more setose than femora; tarsi brown and setose, tarsal claws and pulvilli yellowish to yellowish brown. Dorsum of abdomen white to yellow with numerous, short, longitudinal, red markings. Medial plates 1 and 2 absent; plates 3 5 very similar to fi rst instar except markings more yellow and better defined, plate 6 reduced to transverse band, traversing segments 6 and 7, plates 7 and 8 similar to first instar but each with pale medial spot. Nine lateral plates white with brown margins, sometimes one t o three faint brown spots in white areas. Sterna concolorous with dorsum, red lines and spots slightly less dense medially; medial plates brown with minute

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69 punctures, plates on segments 4 9. Brown markings as follows: circular area surrounding spiracles an d base of trichobothria, crescent shaped markings laterally on each segment corresponding to borders of lateral plates on dorsum; medial plates solid brown and shaped as follows, rounded spot on segment 4, subquadrate markings on segments 5 8 occupying mos t of segment mesially, that on segment 5 about half as broad as other plates, plate on segment 9 U shaped. Spiracles on segments 2 7. Two trichobothria posterior to each spiracle on segments 3 7. Third instar Figure 5 2C Length 3.66 0.14 mm; width 2.36 0.08 mm. Form pyriform to slightly ovoid; brownish black punctures and spots on head and thoracic nota more numerous than second instar. Dorsal surface of head similar to that of second instar except as follows, antennal segment 1 white, dark brown to bl ack band proximally; segment 2 white, brown to reddish brown distally, segments 1 and 2 moderately setose with setal insertions sometimes marked with brown; segment 3 white, reddish brown proximally and distally; segment 4 brown, often reddish brown proxim ally and sometimes distally; ratio of segment lengths approximately 3:6:5:7. Ventral surface of head brown except for yellow gray transverse band reaching from anterad of antennifers nearly to anterior margins of eyes, this band spotted with brown. Thoraci c nota similar to that of second instar except brown areas along posterior margins reduced, particularly on metanotum and mesonotum; mesonotum with medial area more produced posteriorly; metanotum reduced in size. Punctures on pleura more numerous than in second instar. Femora each with proximal two thirds white, distal one third dark brown; tibiae brown, somewhat lighter proximally. Dorsum of abdomen grayish, becoming more green as insects approach ecdysis, with numerous short, longitudinal red markings; m edial plates 3 5 with markings similar to second

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70 instar, often split medially, plate 6 very small, plates 7 and 8 reduced and less defined with paler markings. Lateral plates similar to those of second instar, but with crescent shaped margins thinner and w ith 1 6 small brown punctures. Sterna with medial plates on segments 4 9 varying from similar to those of second instar to almost transparent with brown spots. Fourth instar Figure 5 2D Length 5.40 0.19 mm; width 3.56 0.13 mm. Form ovoid, yellowish gr een dorsally. Similar to third instar except as follows, head with tylus and juga subequal in length; oval spot mediad of eye brown; ocellar spots now usually evident, but partially obscured by brown band on posterior margin of head. Antennal segment 1 yel lowish white to yellowish green with brown spots, often brown proximally; segment 2 yellow to reddish yellow with brown spots; segment 3 white proximally and more yellowish red distally, with faint brown to red spots; segment 4 dark brown, often yellowish brown proximally; ratio of segment lengths approximately 2:7:5:7. Ventral surface of head yellowish except for brown stripe extending from eye to near tip of juga and broad dark band along posterior margin which is interrupted mesially. Rostrum with segmen t 1 yellowish green; segment 2 yellow to brown; segments 3 4 yellowish brown to brown. Thoracic nota with brown borders along posterior margins reduced or absent; humeri with brown punctures more numerous; cicatrices yellowish, often with brown marking mes ially. Brown spots on meso and metanotum similar to third instar or reduced. Meso and metanotal wing pads approximately the same length, extending onto first abdominal segment. Pleura with dark brown spots, lateral half also with dark brown longitudinal vittae. Sterna yellow. Coxae yellow, each with brown band on lateral edge and sometimes central brown spot reduced or absent; trochanters yellow; femora yellow with brown spots at insertions of setae, apices

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71 brownish; tibiae yellowish with red to brown spo ts at insertions of setae, brown distally; tarsi brown, lighter proximally. Dorsum of abdomen yellowish green with dark yellow to green or red markings throughout. Medial plates 2 4 with red to dark brown punctations and brown spots; plates 3 5 similar to third instar, plates 6, 7 and 8 with brown markings reduced to small spots. Lateral plates 2 7 yellowish, each with crescent shaped brown markings thinner; small brown punctures often more numerous (7 12 per segment). Sterna yellowish green. Medial plates reduced to small spots on segments 6, 7, 8, and 9. Fifth instar Figure 5 2E Length 7.35 0.19 mm; width 4.60 0.13 mm. Form ovoid, dorsum of head, thorax and abdomen laterally with relatively dense brown punctures, these larger and more distinct than in fourth instar. Similar to previous instar except as follows, head yellowish green; ocelli evident, reddish. Antennal segments 1 2 yellow with brown spots at setal insertions; segments 3 4 yellow to yellowish red, apex of segment 4 becoming brown; ratio of segment lengths approximately 2:7:5:6. Ventral surface of head yellowish green with sparse brown punctures apically; brown supra antennal vitta distinct. Thoracic nota densely punctured, brown areas surrounding punctures enlarged laterally. Meso and meta notal wing pads subequal in length, extending onto third abdominal segment. Pleura yellow, brown markings reduced compared to previous instar, most punctures almost concolorous with pleural surface, dark spot present at base of each coxa and apex of suprac oxal cleft. Coxae and trochanters yellowish green; both femora and tibiae yellowish green proximally and yellowish red distally, both with brown spots mostly at setal insertions, those on femora

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72 becoming more numerous distally; tarsal segments yellowish re d, segment 2 with apex dark brown. Dorsum of abdomen yellowish green; medial plates 3 5 with white markings more distinct and with red to brown spots, plates 6, 7, and 8 greatly reduced. Lateral plates with numerous brown punctures. Sterna as in previous i nstar, except for red to brown spots reduced or absent, mostly limited to area surrounding spiracles and base of trichobothria; crescent shaped markings greatly reduced. Discussion Based on observations, only 56.4% of the eggs laid hatched into the first i nstar. Incomplete emergence may have attributed to this low percentage of eggs hatching. Some eggs appeared to have been eaten by adults in the cage within 24 hours of being laid. This was obvious because of the egg casings that were recorded in the cages during daily inspection. Euschistus spp. are known to be cannibalistic ( Ruberson et al. 2009 ). Nymphal survival decreased during each stadium. Most insects died in the first, second, and fifth instars. Based on observations, most of these losses resulted f rom incomplete ecdysis. Overall percentage of offspring that reached the adult stage was 33% of the total eggs laid. Nymphs of E. quadrator and E. servus were similar in both their life history and physical appearance (Munyaneza and McPherson 1994). The du ration of the egg and nymphal stages are almost identical between species, with slight variations (Table 5.1). Munyaneza and McPherson (1994) observed that E. servus averages 5.8 0.04 days in the egg stage, whereas I found E. quadrator to remain in the e gg stage for 8.3 0.05 days. Euschistus quadrator remained in the first and second instar for 1.1 and 1.8 days longer than E. servus respectively. However, the third and fifth instars were identical considering the standard errors. The fourth instar for E. quadrator was 1.7 days shorter than that for E. servus The same variations are seen in the range

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73 of days for each stage. Euschistus quadrator had a range of 6 11 days in the egg stage, compared to 5 7 days for E. servus The first and third instars wer e very similar, with 4 8 days and 5 16 days, respectively, for E. quadrator and 4 7 and 5 13 days, respectively, for E. servus The second, fourth and fifth instars had a slightly larger range of 6 12, 6 17 and 9 26 days for E. quadrator compared to 5 8, 7 14 and 8 20 days for E. servus Munyaneza and McPherson (1994) used similar rearing conditions (16L:8D at 23 C), so it is likely that these are species specific differences. The minimum days required for E. quadrator to develop from egg to adult was 36 days, and the maximum was 67 days (Figure 5 3). The overall life cycle is similar for both species. Euschistus servus nymphs are slightly larger than E. quadrator nymphs, though these size differences are only apparent by microscope. Euschistus servus is a pproximately 0.50 mm longer than E. quadrator in the first, second and third instars, and approximately 3.10 mm longer in the fourth and fifth instars. Width for the first, second and third instars of E. servus was 0.14, 0.26 and 0.50 mm greater, respectiv ely, than that of E. quadrator and approximately 2.10 mm for the fourth and fifth instars. Antennal segment lengths and head capsule length and width of E. quadrator nymphs were measured for future aid in identification (Table 5 2). Some notable differenc es are that in the first through third instar of E. quadrator the third antennal segment is white whereas it is brownish red in first through third instars of E. servus The antennal segments are dark in first, second and third instars of E. servus and t he incisures are white (Munyaneza and McPherson 1994). Fourth instars of E. quadrator have dark brown to black tarsi, while in E. servus the tarsi are yellow and brown in the fourth instar. There are two sets of dark spots on the head of fourth instar E. quadrator and only one set of spots on fourth instar E. servus In fifth instars, E. servus has one set of dark spots on the head, which seem to be absent in E. quadrator

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74 fifth instars. The dorso medial abdominal plates in fifth instars of E. quadrator ar e more defined than those of fifth instar E. servus The lateral edges of the head and thorax are a darker brown in E. servus fifth instars. The tip of the fourth antennal segment of fifth instar E. quadrator is darker than that of fifth instar E. servus The lateral plate borders are lighter or absent in E. servus fourth and fifth instars, and a distinct black border is present in fourth and fifth instars of E. quadrator The white line across the eyes of fifth instar E. servus is very well defined, and le ss defined or absent in E. quadrator fifth instars. The differences described above can be used to distinguish E. quadrator from E. servus allowing specific pest management tactics to be developed for both species.

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75 Table 5 1. Duration (in days) of each i mmature stadium of E. quadrator under laboratory conditions Stage Number completing stadium Range Average days** Cumulative mean age Egg 425* 6 11 8.3 0.05 8.3 1 st instar 385 4 8 6.1 0.05 14.3 2 nd instar 343 6 12 7.8 0.07 22.1 3 rd instar 330 5 16 6.8 0.07 28.9 4 th instar 304 6 17 7.6 0.07 36.5 5 th instar 270 9 26 11.2 0.11 47.7 754 eggs were laid ** Means are rounded to the nearest tenth; (

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76 Table 5 2. Head capsule (HC) length and width, and length of antennal segments (A#) of E. quadrator Instar HC Length HC width A1* A2* A3* A4* 1 st 0.38 0.01 0.57 0.01 0.06 0.01 0.13 0.01 0.14 0.01 0.31 0.01 2 nd 0.57 0.02 0.75 0.01 0.10 0.01 0.26 0.01 0.23 0.01 0.46 0.01 3 rd 0.87 0.01 1.04 0. 01 0.15 0.01 0.50 0.02 0.38 0.02 0.65 0.01 4 th 1.22 0.03 1.41 0.01 0.25 0.01 0.87 0.03 0.66 0.02 0.88 0.02 5 th 1.57 0.03 1.81 0.01 0.39 0.01 1.41 0.03 1.05 0.02 1.17 0.02 *A1=distal antennal segment

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77 A B C Figure 5 1. Adult and nymph cage examples. A ) water source, B ) adult stink bug colony cage and C ) nymph cage example (Photo credit by: Sara Brennan)

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78 Figure 5 2. Dorsal (left) and ventral (right) view of immature stages of Euschistus quadrator A) first insta r, B) second instar, C ) third instar, D ) fourth instar, E ) fifth instar

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79 Figure 5 3. Number of nymphs per instar that molted into each subsequent instar during the experiment

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80 CHAPTER 6 GENERAL CONCLUSIONS Blackberry produc tion is increasing in the southeast ( Strik et al. 2007 ). Since blackberries are a relatively new crop to this area, it is expected that the pest complex will be slightly different than the more traditional production areas, such as the northeast and northw est United States. This research focused on stink bug pests of blackberries in Citra, FL. Euschistus quadrator Rolston was one of the most common stink bug species found in blackberries, and is also relatively new to Florida compared to other stink bug spe cies (J. E. Eger, personal communication). There is little information available about E. quadrator Therefore, descriptions of the immature stages of E. quadrator and a life history study were completed to assist with identification of this species in the field. We also assessed monitoring techniques in the field, and attempted to refine laboratory techniques to evaluate pheromone lures used for monitoring stink bugs in blackberry. Finally, a species survey of the stink bug species present in blackberry wa s completed. The results from these studies will help in developing an effective pest management program for stink bugs in commercial blackberry production. Species Survey in Blackberries Euschistus quadrator was the most abundant stink bug found, followed by E. servus E. obscurus T. custator, Proxys punctulatus (Palisot de Beauvois) and the spined soldier bug, P. maculiventris There was a general correlation between the number of stink bugs found on each sampling date with the amount of fruit in each pl ot. As the percent of ripe fruit increased in both the organic and conventional plots, the number of stink bugs also increased. This is the first known record of E. quadrator E. obscurus T. custator P. punctulatus and P. maculiventris in blackberry. Whi le we found several Euschistus spp. that are commonly mentioned in other areas, we did not find either the green stink bug or the southern green stink

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81 bug. It is also interesting to note that E. quadrator was the most abundant stink bug species found, and that so many different Euschistus spp. were found on the blackberries at the same time. Monitoring in Blackberries In the trap comparison experiment, no stink bugs were caught in the tube traps. This indicates that tube traps may not be effective in blackb erry crops. The pyramid trap was more effective in catching stink bugs than the tube trap, either with or without the addition of the Euschistus spp. pheromone. Furthermore, there were no statistical differences between a baited and an unbaited pyramid tra p. In the pheromone comparison experiment, there were no statistical differences in the number of stink bugs caught between the pyramid trap baited with the Trc Pherocon Centrum lure, the Suterra Scenturion lure and an unbaited trap. These results were s upported by results from a Y tube olfactometer assay where there were no statistical differences between either lures and a control, although higher numerical values were recorded with the Trc lure. This indicates that both lures are most likely ineffect ive in the field. This research may provide information for growers who are considering the purchase of available lures as to which lure is more practical and whether a lure is needed for their field setting. Species found in field experiments include E. q uadrator E. servus E. obscurus (Palisot de Beauvois), Thyanta custator (F.), E. ictericus (L.) and Podisus maculiventris Say. Stink bugs appear to colonize in blackberry bushes when berries are mid ripe to fully ripe. Life History and Taxonomy of E. quad rator Only 56.4% of the eggs laid hatched into the first instar, and 33% of the total eggs laid reached the adult stage. Incomplete emergence from eggs and incomplete ecdysis between instars may have attributed to this low percentage of survival. The overa ll life history and

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82 physical appearance of E. quadrator nymphs are very similar to the brown stink bug, Euschistus servus (Say), an economically important pest (Munyaneza and McPherson 1994). Euschistus quadrator remained in the egg stage for approximately 2.5 days longer than E. servus The first and second instars for E. quadrator were 1.1 and 1.8 days longer, respectively, than E. servus However, the duration of the third and fifth instars was identical between species. The fourth instar for E. quadrato r was 1.7 days shorter than that for E. servus The same small variations are seen in the range of days for each stage. At 25 C, the minimum duration from egg to adult for E. quadrator was 36 days, and the maximum was 67 days. Euschistus servus nymphs are slightly larger than E. quadrator nymphs. Some of the more notable differences are that in the first through third instar of E. quadrator the third antennal segment is white whereas it is brownish red in first through third instars of E. servus Fourth i nstar nymphs of E. quadrator have dark brown to black tarsi, while in fourth instar E. servus the tarsi are yellow and brown. There are two sets of dark spots on the head of fourth instar E. quadrator and only one set of spots on fourth instar E. servus In fifth instar nymphs, E. servus has one set of dark spots on the head, which seem to be absent in E. quadrator fifth instars. The white line across the eyes of the fifth instars of E. servus is very well defined, and less defined or absent in fifth inst ar E. quadrator The differences described above can be used to distinguish E. quadrator from E. servus allowing specific pest management tactics to be developed for individual species.

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83 LIST OF REFERENCES Aldrich, J. R., M. P. Hoffmann, J. P. Kochansky, W. R. Lusby, J. E. Eger, and J. A. Payne. 1991. Identification and attractiveness of a major pheromone component for Nearctic Euschistus spp. stink bugs (Heteroptera: Pentatomidae). Environ. Entomol. 20: 477 483. Anderson, P.C., J. G. Williamson, and T. E Crocker. 2011. Sustainability assessment of fruit and nut crops in north Florida and north central Florida. University of Florida IFAS Extension HS765. ( http://edis.ifas.ufl.edu/mg367 ) Anonymous. 2008. Berr ies Northwest. ( http://www.berriesnw.com/BerryDisordersList.asp ) Ashmead, W. H. 1887. Report on insects injurious to garden crops in Florida. Bull. Div. Entomol. U.S. Dept. Agric. 14: 9 29. Barber, H. G. 1914. Insects of Florida. II. Hemiptera. Bull. Amer. Mus. Nat. Hist. 33: 495 535. Borden, A. D., H. F. Madsen, and A. H. Retan. 1952. A stink bug, Euschistus conspersus destructive to deciduous fruits in California. J. Econ. Entomol. 45: 25 4 257. Bowen Forbes, C. S., Y. Zhang, and M. G. Nair. 2008. Anthocyanin content, antioxidant, anti inflammatory and anticancer properties of blackberry and raspberry fruits. J. Food Compos. Anal. Bowling, C. C. 1979. The stylet sheath as an indicator of feeding activity of the rice stink bug. J. Econ. Entomol. 72: 259 260. Bowling, C. C. 1980. The stylet sheath as an indicator of feeding activity by the southern green stink bug on soybeans. J. Econ. Entomol. 73: 1 3. Boyd, M. L., and D. J. Boethel. 1998 Susceptibility of predaceous Hemipteran species to selected insecticides on soybean in Louisiana. J. Econ. Entomol. 91(2): 401 409. Brambila, J. 2007. Heteroptera of Concern to Southeastern U.S. pp. 2 3. In Southern Plant Diagnostic Network Invasive Art hropod Workshop, May 7 9, 2007, vol 9(6).Clemson, South Carolina, USA. J. Insect Sci. Bundy, C. S., and R. M. McPherson. 2000a. Morphological examination of stink bug (Heteroptera: Pentatomidae) eggs on cotton and soybeans, with a key to genera. Ann. Ent omol. Soc. Am. 93: 616 624. Bundy, C. S., and R. M. McPherson. 2000b. Dynamics and seasonal abundance of stink bugs (Heteroptera: Pentatomidae) in a cotton soybean ecosystem. J. Econ. Entomol. 93(3): 697 706. Buntin, G. D., and J. K. Greene. 2004. Abunda nce and species composition of stink bugs (Heteroptera: Pentatomidae) in Georgia winter wheat. J. Entomol. Sci. 39(2): 287 290.

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84 Buschman, L. L., and W. H. Whitcomb. 1980. Parasites of Nezara viridula (Hemiptera: Pentatomidae) and other Hemiptera in Florida Fla. Entomol. 63: 154 162. Butterworth, J. R., and E. D. Morgan. 1971. Investigations of the locust feeding inhibition of the seeds of the neem tree, Azadirachta indica J. Insect Physiol. 17: 969 977. Casida, J. E. 1980. Pyrethrum flowers and pyrethro id insecticides. Environ. Health Persp. 34: 189 202. Cassidy, T. P., and T. C. Barber. 1939. Hemipterous insects of cotton in Arizona: their economic importance and control. J. Econ. Entomol. 32(1): 99 106. Cherry, R. H., and A. Wilson. 2011. Flight acti vity of stink bug (Hemiptera: Pentatomidae) pests of Florida rice. Fla. Entomol. 94(2): 359 360. Chyen, D., M. E. Wetzstein, R. M. McPherson, and W. D. Givan. 1992. An economic evaluation of soybean stink bug control alternatives for the Southeastern Unit ed States. Southern J. Agric. Econ. 24: 83 94. Clark, J. R. 1992. Blackberry production and cultivars in North America east of the Rocky Mountains. Fruit Varieties J. 46: 217 222. Clark, J. R. 2005. Changing times for eastern United States blackberries. HortTechnology. 15(3): 491 494. 1296. 260. Clark, J. R., and J. N. Moore. 2008. 1899. Cottrell, T. E. 2001. Improved trap capture of Euschistus servus and Euschistus tristigmus (Hemiptera: Pentatomidae) in pecan. Fla. Entomol. 84: 731 732. Crandall, P. C. 1995. Bramble productio n: the management and marketing of raspberries and blackberries. Food Products Press, Binghamton, NY. Daugherty, D. M. 1967. Pentatomidae as vectors of yeast spot disease of soybeans. J. Econ. Entomol. 60: 147 52. DeFrancesco, J., W. Parrott, and J. Jenk ins. 2002. Crop profile for blackberry in Oregon. ( http://www.ipmcenters.org/cropprofiles/docs/ORblackberries.pdf ) Eger, J. E., Jr., and J. R. Ables. 1981. Parasitism of Penta tomidae by Tachinidae in South Carolina and Texas. Southwest. Entomol. 6(1): 28 33.

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85 Ellis, M. A., R. H. Converse, R. N. Williams, and B. Williamson. 1991. Compendium of raspberry and blackberry diseases and insects. APS Press, St. Paul, MN. 122 pp. Envir onmental Protection Agency (EPA). 1991. Labeling Requirements for Pesticides and Devices. Code of Federal Regulations, Title 40, Part 156. Esquivel, J. F., R. M. Anderson, and R. E. Droleskey. 2009. A visual guide for identification of Euschistus spp. (He miptera: Pentatomidae) in central Texas. Southwest. Entomol. 34(4): 485 488. Esselbaugh, C. O. 1946. A study of the eggs of the Pentatomidae (Hemiptera). Ann. Entomol. Soc. Am. 39(4): 667 691. Flint, M. L., and P. Gouveia. 2001. IPM in practice: principl es and methods of integrated pest management. University of California Division of Agriculture and Natural Resources, Oakland, CA. Fontes, E. M. G., D. H. Habeck, and F. Slanksky, Jr. 1994. Phytophagous insects associated with goldenrods ( Solidago spp.) i n Gainesville, Florida. Fla. Entomol. 77(2): 209 221. Frost, S. W. 1979. A preliminary study of North American insects associated with elderberry flowers. Fla. Entomol. 62(4): 341 355. Gerdeman, B. S., L. K. Tanigoshi, and J. R. Bergen. 2005. Western Was hington field guide to common small fruit root weevils. WSU Extension. ( http://cru.cahe.wsu.edu/CEPublications/eb1990/eb1990.pdf ) Gomez, C., and R. F. Mizell III. 2009. Black Stink B ug Proxys punctulatus (Palisot) (Insecta: Hemiptera: Pentatomidae). University of Florida IFAS Extension EENY 432. ( http://edis.ifas.ufl.edu/in795 ) Greene, J. K., S. G. Turnipseed, M. J. Sullivan, and O. L. M ay. 2001. Treatment thresholds for stink bugs (Hemiptera: Pentatomidae) in cotton. J. Econ. Entomol. 94: 403 409. Henry, T. J., and R. C. Froeschner. 1998. Catalog of the Heteroptera, or True Bugs, of Canada and the Continental United States. E. J. Brill. Leiden. Herbert, J. J., and M. D. Toews. 2011. Seasonal abundance and population structure of brown stink bug (Hemiptera: Pentatomidae) in farmscapes containing corn, cotton, peanut, and soybean. Ann. Entomol. Soc. Am. 104(5): 909 918. Hill, S. O. 1938. Important pecan insects of northern Florida. Fla. Entomol. 21(1): 9 13. Hogmire, H. W., and T. C. Leskey. 2006. An improved trap for monitoring stink bugs (Heteroptera: Pentatomidae) in apple and peach orchards. J. Entomol. Sci. 41(1): 9 21.

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86 Hokkanen, H M. T. 1991. Trap cropping in pest management. Annu. Rev. Entomol. 36: 119 138. Hopkins, B. W. 2005. Species composition and seasonal abundance of stink bugs in cotton in the lower Texas Gulf coast and the virulence of Euschistus species to cotton. M.S. thesis, Texas A&M University, College Station. Hopkins, B. W., A. E. Knutson, J. S. Bernal, M. F. Treacy, and C. W. Smith. 2010. Species composition, damage potential, and insecticide susceptibility of stink bugs in cotton in the Lower Gulf Coast Region o f Texas. Southwest. Entomol. 35(1): 19 32. Hopkins, B. W., J. S. Bernal, and A. E. Knutson. 2005. Euschistus quadrator (Hemiptera: Pentatomidae): a new pest in lower Texas Gulf coast cotton. Proc. Beltwide Cotton Conf. 1480 1485. Jennings, D. L, H. A. D aubeny, and J. N. Moore. 1991. Blackberries and raspberries (Rubus). Acta Hortic. 290: 331 392. Johnson, D., and B. A. Lewis. 2003. Crop profile for blackberries in Arkansas. ( htt p://www.ipmcenters.org/CropProfiles/docs/ARblackberry.pdf ) Jones, D. B., and R. H. Cherry. 1986. Species composition and seasonal abundance of stink bugs (Heteroptera: Pentatomidae) in southern Florida rice. J. Econ. Entomol. 79: 1226 1229. Kamminga, K. L., D. A. Herbert, Jr., T. P. Kuhar, S. Malone, and H. Doughty. 2009. Toxicity, feeding preference, and repellency associated with selected organic insecticides against Acrosternum hilare and Euschistus servus (Hemiptera: Pentatomidae). J. Econ. Entomol. 102(5): 1915 1921. Koppel, A. L., D. A. Herbert, Jr., T. P. Kuhar, and K. Kamminga. 2009. Survey of stink bug (Hemiptera: Pentatomidae) egg parasitoids in wheat, soybean, and vegetable crops in southeast Virginia. Environ. Entomol. 38(2): 375 379. Kottek M., J. Grieser, C. Beck, B. Rudolf, and F. Rubel. 2006. World Map of Kppen Geiger Climate Classification updated. Meteorol. Z. 15(3): 259 263. Krupke, C. H., J. F. Brunner, M. D. Doerr, and A. D. Kahn. 2001. Field attraction of the stink bug Euschistus conspersus (Hemiptera: Pentatomidae) to synthetic pheromone baited host plants. J. Econ. Entomol. 94: 1500 1505. Ladd Jr., T. L., M. Jacobson, and C. R. Buriff. 1978. Japanese beetles: extracts from neem tree seeds as feeding deterrents. J. Econ. Entomol 71: 810 813. Lampson, B., Y. Han, A. Khalilian, J. Greene, R. W. Mankin, and E. Foreman. 2010. Characterization of substrate borne vibrational signals of Euschistus servus (Heteroptera: Pentatomidae). Amer. J. Agric. Biol. Sci. 5(1): 32 36.

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91 Tillman, P. G., and B. G. Mullinix, Jr. 2004. Comparison of susceptibility of pest Euschistus servus and predator Podisus maculiventris (Heteroptera: Pentatomidae) to selected insecticides. J. Econ. Entomol. 97: 800 806. Tillman, P. G., J. R. Aldrich, A. Khrimian, and T. E. Cottrell. 2010. Pheromone attraction and cross attraction of Nezara Acro sternum and Euschistus spp. stink bugs (Heteroptera: Pentatomidae) in the field. Environ. Entomol. 39(2): 610 617. Tillman, P. G., T. D. Northfield, R. F. Mizell, and T. C. Riddle. 2009b. Spatiotemporal patterns and dispersal of stink bugs (Heteroptera: Pentatomidae) in peanut cotton farmscapes. Environ. Entomol. 38(4): 1038 1052. Todd, J. W. 1982. Effects of stinkbug damage on soybean quality, pp. 46 51. In J.B. Sinclair and J.A. Jackobs, (eds.), Soybean Seed Quality and Stand Establishment, INTSOY Seri es Number 22, College of Agriculture,University of Illinois at Urbana Champaign. Todd, J. W., and D. C. Herzog. 1980. Sampling phytophagous Pentatomidae on soybean, pp. 438 478. In M. Kogan and D. C. Herzog (eds.), Sampling Methods in Soybean Entomology. Springer Verlag, New York, New York. Toews, M. D., and W. D. Shurley. 2009. Crop juxtaposition affects cotton fiber quality in Georgia farmscapes. J. Econ. Entomol. 102(4): 1515 1522. Townsend, L. H., and J. D. Sedlacek. 1986. Damage to corn caused by Eu schistus servus E. variolarius and Acrosternum hilare (Heteroptera: Pentatomidae) under greenhouse conditions. J. Econ. Entomol. 79: 1254 1258. Turner, J. L., and O. E. Liburd. 2007. Insect management in blueberries. University of Florida IFAS Extension ENY 411. ( http://edis.ifas.ufl.edu/ig070 ) Turnipseed, S. G., and M. Kogan. 1976. Soybean entomology. Annu. Rev. Entomol. 21: 247 282. (USBC) United States Bureau of the Census. 1952. U.S. Census of agricult ure: 1950. Volume 1, part 18. Counties and state economic areas. U.S Government Printing Office. Washington, DC. (USDA) United States Department of Agriculture National Agricultural Statistics Survey. 1994. 1992 Census of agriculture. Volume 1, part 9. Fl orida state and county data. USDA. Washington, DC. (USDA) United States Department of Agriculture National Agricultural Statistics Survey. 1999. 1997 Census of agriculture. Volume 1, part 9. Florida state and county data. USDA. Washington, DC.

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93 BIOGRAPHICAL SKETCH Sara A. Brennan was born in Camden, New Jersey in 1984. She was raised in Vero Beach, Florida, and attended the University of Florida in 2002. She earned a Bachelor of Art s in 2006 where she majored in classical s tud ies. In 2009, she changed her career focus and began her Liburd. After graduating, she hopes to take six months to a year off before beginning her Ph.D. Her fu ture study and career interests include sustainable urban agriculture, with a sub focus on the social, economic and government policy aspects of agriculture.