docLife History and Laboratory Rearing of Bagrada hilaris (Hemiptera
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Life History and Laboratory Rearing of Bagrada hilaris (Hemiptera
Annals of the Entomological Society of America Advance Access published May 28, 2015 MORPHOLOGY, HISTOLOGY, AND FINE STRUCTURE Life History and Laboratory Rearing of Bagrada hilaris (Hemiptera: Heteroptera: Pentatomidae) with Descriptions of Immature Stages M. E. TAYLOR,1 C. S. BUNDY,1,2 AND J. E. McPHERSON3 Ann. Entomol. Soc. Am. 1–16 (2015); DOI: 10.1093/aesa/sav048 ABSTRACT Bagrada hilaris (Burmeister) (Hemiptera: Heteroptera: Pentatomidae) is an Old World pest recently established in North America. Literature on the life history and immature descriptions of B. hilaris is scattered and variable in content. Therefore, we conducted a study of this insect’s life history in southern New Mexico from January 2012 to August 2014, reared the bugs in the laboratory, and described the immature stages. Two primary host plants, London rocket (Sisymbrium irio L., a winter annual) and mesa pepperwort (Lepidium alyssoides A. Gray, a summer perennial), were sampled weekly to record numbers of the various life stages and behavioral activities; broccoli (Brassica oleracea L.) also was sampled for one season. Adults were found continuously throughout the year. They deposited eggs individually in the soil near the bases of their host plants from February through October. Nymphs were found every month of the year. The number of generations per year was difficult to determine due to such factors as extreme overlap of generations and a lack of reproductive diapause. However, the data roughly suggest this species is bivoltine, although there is some evidence of a partial third generation. The bug also was reared from egg to adult under controlled laboratory conditions on fruiting structures of mesa pepperwort at 25 6 0.01 C under a photoperiod of 14:10 (L:D) h. The incubation period averaged 7.45 d. The five stadia averaged 3.35, 7.08, 6.39, 7.33, and 10.25 d, respectively. Instars can be distinguished readily by differences in several morphological features in addition to body size and coloration. KEY WORDS Bagrada hilaris, Pentatomidae, life history, immature descriptions The family Pentatomidae, which occurs worldwide, contains 900 genera and >4,700 species (Henry 2009). It is represented in America north of Mexico by 60 genera and >200 species (Froescher 1988) including Bagrada hilaris (Burmeister) (Halbert and Eger 2010). Bagrada is primarily an Old World genus with three subgenera and 16 species (Rider 2006). Only B. hilaris occurs in both the Old and New Worlds (Halbert and Eger 2010). B. hilaris is considered native to Africa, India, Pakistan, Southeast Asia, and southern Europe, where it is a pest of cole crops (Brassicaceae) (Arakelian 2008– 2009, Reed et al. 2013, Taylor et al. 2014). It first was collected in the United States from Los Angeles County, CA, in 2008 (Garrison 2008–2009) and has spread north and south in California and east through Nevada, Utah, Arizona, and New Mexico to Texas (Reed et al. 2013); it now is established in Mexico (Sa´nchez-Pen˜a 2014). 1 Department of Entomology, Plant Pathology, and Weed Science, New Mexico State University, Las Cruces, NM 88003. 2 Corresponding author, e-mail: cbundy@nmsu.edu. 3 Department of Zoology, Southern Illinois University, Carbondale, IL 62901. Although best known as a pest of cole crops, B. hilaris has been reported from at least 76 species in 20 plant families from Poaceae to the Solanaceae (Table 1). The bugs feed predominantly on leaves and young seeds. Severe host damage can be caused by feeding on the apical meristem or cotyledons (Palumbo and Natwick 2010). B. hilaris has been reared in the laboratory under variable conditions. Azim and Shafee (1986) reported an incubation period of 2–5 d and nymphal stadia of 2–3 d each for the first through fourth instars and 3–4 d for the fifth instar on cabbage (Brassica oleracea L.). Verma et al. (1993) reported stadia for the first through fifth instars of 3.33, 4.00, 4.31, 4.54, and 3.82 d, respectively, on Indian mustard [Brassica juncea (L.)], under controlled conditions. Singh and Malik (1993) reared the bugs on Indian mustard seeds in the laboratory at different times of year reporting an incubation period and nymphal stadia (first–fifth instars combined), respectively, of 6.22 and 14–22 d in April (25.5–34 C), 3.28 and 14–20 d in May (28–30 C), and 6.27 and 29–37 d (28 C; no month given). A few illustrations and descriptions of the egg and immature stages have been published for B. hilaris [or its synonyms: Bagrada cruciferarum Kirkaldy and Bagrada picta (F.)]. Superficial illustrations were provided by Hutson (1935) (egg, second through fifth instars, and adult) and Narayanan (1958) (egg, first C The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America. V All rights reserved. For Permissions, please email: journals.permissions@oup.com 2 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Table 1. Plant associations or feeding records for B. hilaris Family Annonaceae Apiaceae Asteraceae Brassicaceae Caricaceae Capparaceae Chenopodiaceae Compositae Convolvulaceae Cucurbitaceae Euphorbiaceae Fabaceae Malvaceae Poaceae Species Asimina triloba (L.) Daucus carota L. Bidens pilosa L. Cynara cardunculus var. scolymus Dendranthema grandiflorum (Ramat.) Kitamura Helianthus annuus L. Lactuca sativa L.c Schkuhria pinnata (Lam.) Kuntze ex Thell. Sonchus arvensis L. Barbarea sp. Brassica compestris L. Brassica juncea (L.) Czern. Brassica napobrassica (L.) Mill. Brassica napus L. Brassica oleracea L. var. italica Plenck. Brassica oleracae L. var. acephala D.C. Brassica oleracea L. var. botrytis subvar. cauliflora D.C. Brassica oleracea L. var. capitata L Brassica oleracea var. gongylodes Brassica oleracea L. var. gemmifera D.C. Brassica rapa subsp. Pekinensis Rupr. Brassica rapa L. subsp. oleifera (D.C.) Metzg. Brassica rapa var. rapa L. Capsella busa-pastoris (L.) Medikus Eruca sativa Mill. Hirschfeldia incana (L.) Lagrese-Fossat Iberis spp. Lepidium alyssoides A. Gray Lepidium latifolium L. Lepidium capense Thunb. Lobularia matitima (L.) Desvaux Mathiola spp. Raphanus sativus L. Raphanus raphanistrum L. Sisymbrium irio L. Sisymbrium capense Thunb. Carica papaya L. Capparis spinosa L. Beta vulgaris L. Chenopodium album L. Spinacia oleracea L.c Dahlia sp. Convolvulus arvensis L. Citrullus lanatus (Thunb.)c Cucumis melo L. subsp. melo var. cantalupo Ser. Euphorbia hirta L. Arachis hypogaea L. Indigofera sp. Pisum sativum (L.) Vigna mungo (L.) Hepper Vigna radiata (L.) R. Wilczek Abelmoschus esculentus L. Alcea sp. Gossypium hirsutum L. Avena sativa L. Cynodon dactylon (L.) Pers. Cyperus rotandus L. Dactyloctenum aegyptium (L.) Beauv. Hordeum vulgare L. Oryza sativa L. Pennisetum glaucum (L.) R. Br. Saccharum officinarum L. Saccharum spontaneum L. Sorghum bicolor (L.) Moench subsp. drummondii (Nees ex Steud.) de Wet & Harlan Common name Locationa Referenceb pawpaw carrot black jack artichoke chrysanthemum NG NG South Africa NG NG Gunn 1918 Gunn 1918 Gunn 1918 Gunn 1918 Gunn 1918 sunflower lettuce pinnate false threadleaf Field sow thistle, corn sow thistle winter cress wild rape Indian mustard rutabaga rapeseed, canola broccoli, broccoflower kale, collards cauliflower USA NG South Africa India South Africa South Africa Sri Lanka USA (AZ) India USA (CA) USA (CA) Sri Lanka Bundy et al. 2012 Gunn 1918 Gunn 1918 Singh and Malik 1993 Gunn 1918 Gunn 1918 Hutson 1935 Palumbo and Natwick 2010 Singh and Malik 1993 Arakelian 2008–2009 Arakelian 2008–2009 Hutson 1935 cabbage kohlrabi, knoll khol Brussels sprouts Chinese cabbage field mustard turnip shepherd’s purse salad rocket, arugula shortpod mustard candytuft mesa pepperwort perennial pepperweed cape pepper-grass sweet alyssum stock radish jointed charlock London Rocket Cape mustard papaya caper sugarbeet lamb’s quarters spinach dahlia field bindweed watermelon cantaloupe NG India USA USA (AZ) India NG USA (AZ) South Africa USA (AZ) USA USA (NM) USA (NM) South Africa NG NG NG South Africa USA (AZ) South Africa USA (CA) Italy NG India USA (AZ) NG India USA (AZ) USA (AZ) Gunn 1918 Rakshpal 1949 Bealmear et al. 2012 Palumbo and Natwick 2010 Azim and Shafee 1986 Gunn 1918 Reed et al. 2013 Gunn 1918 Reed et al. 2013 Gunn 1918 Bundy et al. 2012 Bundy et al. 2012 Gunn 1918 Gunn 1918 Gunn 1918 Gunn 1918 Gunn 1918 Reed et al. 2013 Gunn 1918 Arakelian 2008–2009 Ahuja et al. 2008 Gunn 1918 Singh and Malik 1993 Palumbo and Natwick 2010 Gunn 1918 Singh and Malik 1993 Palumbo and Natwick 2010 Palumbo and Natwick 2010 pill-pod spurge peanut, groundnut Indigo pea black gram green gram okra hollyhock cotton oats Bermuda grass nut grass Egyptian crowfoot grass India Africa, Asia India NG India India India NG Africa, India NG USA India India Singh and Malik 1993 Hill 1975 Narayanan 1954 Gunn 1918 Gupta and Gupta 1970 Gupta and Gupta 1970 Singh and Joshi 2004 Gunn 1918 Hill 1975 Gunn 1918 Reed et al. 2011 Singh and Malik 1993 Sandhu 1975 barley rice pearl millet sugarcane Kans grass (kahi) Sudan grass NG India India India India USA Gunn 1918 Rakshpal 1949 Gupta and Gupta 1970 Narayanan 1954 Sandhu 1975 Reed et al. 2011 (continued) 2015 TAYLOR ET AL.: LIFE HISTORY AND LABORATORY REARING OF B. hilaris 3 Table 1. Continued Family Polygonaceae Rhamnaceae Rubiaceae Solanaceae Tropaeolaceae Zygophylaceae Species Sorghum halepense (L.) Pers. Sorghum vulgare (L.) Pers. Triticum aestivum L. Zea mays L. Polygonum plebeium R.Br. Ziziphus rotundifolia (Burm. f.) Wight & Arn. Cofea spp. Physalis peruviana L. Solanum tuberosum L. Nasturtium integrifolium (Nutt.) Kuntze Tribulus terrestris L. Common name Locationa Referenceb Johnson grass sorghum wheat maize knotweed wild jujube India India South Africa India India India Sandhu 1975 Sandhu 1975 Gunn 1918 Halbert and Eger 2010 Singh and Malik 1993 Singh and Malik 1993 coffee cape gooseberry Potato nasturtium USA NG India South Africa Rakshpal 1949 Gunn 1918 Hill 1975 Gunn 1918 puncturevine India Sandhu 1975 a NG: location not given. b Only reference of first report of host plant given here. c Host records where damage to the plant was not observed. through fifth instars, and adult). Brief descriptions of the egg and first through fifth instars were reported by Rakshpal (1949), Verma et al. (1993), and Azim and Shafee (1986). Azim and Shafee also included illustrations and a key to the nymphal instars. Several Old World reports are available on the natural enemies of B. hilaris. Eggs are attacked by scelionid parasitoids (Hymenoptera) including Gryon karnalense (Chacko and Katiyar) (as Hadrophanurus karnalensis) (Chacko and Katiyar 1961), Telenomus samueli (Mani) (as Liophanurus samueli) (Mani 1941, Mani and Sharma 1982), Trissolcus spp. (Cheema et al.1973, Ghosal et al. 2005), and Tiphodytes sp. (Samuel 1949). Adults are attacked by the tachinid parasitoids (Diptera) including Alophora pusilla Meigan (Rakshpal 1949, 1954; Crosskey 1976; Azim and Shafee 1986), Hyalomya pusilla Meigan (Cheema et al. 1973), and A. indica (Mesnil) (Cheema et al. 1973, Crosskey 1976). Rakshpal (1954) suggested that the sex of the bug attacked determined the sex of A. pusilla. Thakar et al. (1969) reported the predatory mite Bochartia sp. (Acarina: Erythraeidae) feeding on nymphs and adults. Although numerous studies on the biology of B. hilaris have been published for the Old World, little information is available for North America. In south central Asia, adults have been collected throughout the year (Batra 1958, Narayanan 1958, Atwal 1959). They were most active from October through March feeding on mature pods of winter crops. During the spring, they were found beneath debris in harvested fields (Sandhu 1975). In India, Singh and Malik (1993) also reported year-round survival of adults with peak populations during seedling stages from October to November and another peak during harvest from March to April. Populations were relatively low from December to January when temperatures were lowest. In the New World, Garrison (2008–2009) reported adults and nymphs in June and September to November in California feeding on rape (Brassica napus L.), Alyssum sp., “daikons,” turnips, and broccoli (B. oleracea). He also stated it had spread to the Yuma region of Arizona where it fed on Brassica weeds, seed crops, canola, and cotton. Bundy et al. (2012) reported populations of nymphs and adults from several localities in New Mexico on a variety of host plants, including mesa pepperwort (Lepidium alyssoides A. Gray), from April through September (2010–2011). Reed et al. (2013) reported two main peaks (life stages not given) in B. hilaris populations in southern California, April to May and September to October, with adults overwintering in the soil near a food source. Palumbo (2013) found adult survival throughout the year in Arizona with peaks from September to October and March to April on a variety of host plants including broccoli and cabbage. Among the localities mentioned by Bundy et al. (2012) was Las Cruces. Here, high numbers were observed on mesa pepperwort, suggesting that a detailed life history study was possible. Presented here is the life history of B. hilaris in and around Las Cruces including information on laboratory rearing under controlled conditions and descriptions and illustrations of the immature stages. Materials and Methods Life History. A field survey was conducted from January 2012 to August 2014 at several sites in and around Las Cruces, NM. Sampling primarily involved two host plants: London rocket (Sisymbrium irio L.), a winter annual species, and mesa pepperwort, a summer perennial species. For London rocket, collecting was primarily from December through June and for mesa pepperwort, May through November; however, a few individuals were collected outside these periods. Although London rocket was one of the two primary hosts, no specimens were collected from this host during the beginning of this project (15 January through 25 May 2012), even though it was sampled extensively during this time. Responding to a report by a stakeholder of these bugs on broccoli, we began sampling this plant on 7 November 2012, which continued through the third week in March when the plants had senesced. Also added for sampling on 5 December 2012 was a patch of London rocket that was infested with B. hilaris near the broccoli field, which continued through 15 May 2013 when plants were destroyed by the grower. 4 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Counts of all life stages and notes on the bugs’ activities were taken weekly. Samples of mesa pepperwort consisted of six plants per field site utilizing the beatbucket technique (modified from Bundy and McPherson 2009). Leaves from a single plant were shaken rapidly over a bucket (38.8 by 31.9 by 14.4 cm), and dislodged insects were counted, determined to instar(s), if possible, and released. Individuals that could not be determined to instar in the field were taken to the laboratory for closer examination. During the winter months, samples of mesa pepperwort were expanded to include observations of the bugs on leaf litter and at the bases of the plants, which remained green throughout the winter months. Samples of London rocket and broccoli consisted of whole plant samples (six plants per species) rather than the beat-bucket technique. For London rocket, the beat-bucket technique was ineffective for plants, which varied in size significantly from winter through spring. For broccoli, the beat bucket technique was too damaging to the plant. During weekly sampling of various hosts, bugs often were observed on the soil near the bases of the plants. Therefore, small areas of soil within a radius of 20 cm from the bases were included during sampling to obtain a better representation of the population. For all sampling techniques, counts of adults and each immature stage were recorded, and plant material was inspected for the presence of eggs. Representative samples of nymphs were preserved in 80% ethanol (EtOH) to check field determinations and for use in immature descriptions (see below). In late February 2013, soil samples from around the perimeter of plants were collected in hopes of recovering eggs. Soil (1 liter, total) was collected from the base of each of six plants using a garden spade to scrape the loose soil (1.5 cm deep), taken to the laboratory in plastic bags, and washed through a set of sieves (203.2 mm in diameter, 50.8 mm in depth): number 10 (2.0 mm, mesh size), number 20 (0.83 mm, mesh size), and number 35 (0.50 mm, mesh size). Debris from the last sieve (number 35) was placed in a large dish (15 cm in diameter and 2 cm in depth) with water (10 ml), and the contents were examined for eggs. Laboratory Rearing. Adults (100 females, 100 males) were collected from mesa pepperwort in and around Las Cruces from early August to mid-October 2012, taken to the laboratory, and placed in an ovipositional cage. The cage consisted of a large terrarium (61 by 32 by 41 cm) lined with paper toweling (to absorb excess water) and provided with cuttings (30 cm in length) of mesa pepperwort with fruiting structures. Cuttings were inserted into a block of floral foam (7 by 7 by 5.5 cm), which previously had been placed in a small plastic cup (350 ml) filled with distilled water and covered with paper toweling to avoid excess moisture. A small petri dish (9 cm in diameter and 1.5 cm in depth) with distilled water was added to the cage to provide a water source and filled with cotton balls to prevent the bugs from drowning. One or two narrow cheesecloth strips (50.8 by 2 cm) were draped over the plants and served as ovipositional sites. Adults were transferred to a new ovipositional cage daily and the old plant material and toweling examined for eggs. The eggs were removed with a paint brush or fine-tipped forceps and placed on moistened filter paper in petri dishes (10 cm in diameter and 2 cm in depth). The old cages then were cleaned with soap and water to ensure no eggs remained. Nymphs were kept in petri dishes similar to those for eggs but provided with cuttings (3 cm) of the fruiting structures of mesa pepperwort for food. Petri dishes were examined daily, molts recorded, and exuviae removed. Nymphs were grouped by molting dates to determine stadia. Filter paper was moistened daily, and food was replaced as needed, approximately every 2 d. Eggs, nymphs, and adults were maintained in the laboratory in an incubator at 25 6 0.01 C under a photoperiod of 14:10 (L:D) h. Description of Immature Stages. Descriptions of the egg and instars are based on 10 individuals. Eggs and first instars were obtained in the laboratory from field-collected females; second through fifth instars were field-collected. All immature stages were preserved in 80% EtOH. Illustrations were made on a lightbox from digital photographs taken on a Canon EOS 5D mark II with the Passport system. Digital renderings were created using Adobe Illustrator CS6 and Photoshop CS6. Measurements of most structures (in mm) were made using an ocular micrometer; those for micropylar processes (in mm) were made from scanning electron micrographs. Scanning electron micrographs were used in the description of the egg. Eggs were fixed 2.5% glutaraldehyde, rinsed with 0.1 M imidazole buffer, and run through a critical point dryer. They were mounted on a carbon adhesive tab, sputter-coated with gold, and examined with a scanning electron microscope (S3400N II, Hitachi High Technologies, Pleasanton, CA) at an accelerating voltage of 10 kV. Statistics. Measurements are expressed as means 6 SE; SEs <0.005 are listed as 0.00. Data on total developmental time of male and female bugs were analyzed with the SAS (SAS Institute 2002–2008) TTEST procedure. Level of significance selected was 0.05. Voucher Specimens. Selected samples of eggs and instars have been vouchered in the New Mexico State Arthropod Museum in Las Cruces, NM. Results and Discussion Life History. Adults (n ¼ 8,264) and nymphs (18,060) of B. hilaris were found continuously throughout the year, including the winter months, on or near their host plants (Figs. 1 and 2). Mating pairs (n ¼ 1,687) were found continuously (at least one pair each week) through the year on mesa pepperwort (n ¼ 1,294), peaking from mid-June to early October; and discontinuously on London rocket (n ¼ 393), peaking from early January to mid-May. (Note: percentages of life stages at low levels are not visible for some dates on the life history graphs [Figs. 1–6]). 2015 TAYLOR ET AL.: LIFE HISTORY AND LABORATORY REARING OF B. hilaris / / / / / Jan Feb Mar Apr May June July Aug Sept Oct 5 / // / Nov Dec 50 25 ADULT 0 (N=8264) 25 50 25 EGG 0 (N=642)25 50 1ST 25 INSTAR 0 (N=2715)25 50 2ND 25 INSTAR 0 (N=4249)25 50 3RD 25 INSTAR 0 (N=4290)25 50 4TH 25 INSTAR 0 (N=3061)25 50 5TH 25 INSTAR 0 (N=3745)25 50 Fig. 1. Composite field life cycle of B. hilaris on mesa pepperwort, London rocket, and broccoli in Las Cruces, NM, 2012–2014. Percentage in each sample of total individuals of each stage. Percentages less than 5% may not be visible due to size of figure. Top horizontal bar represents actively growing periods of each host plant: gray ¼ mesa pepperwort; white diagonal stripes ¼ mesa pepperwort þ broccoli overlap; black diagonal stripes ¼ broccoli þ London rocket overlap; black ¼ London rocket þ mesa pepperwort overlap. / / / / / Jan Feb Mar Apr May June July Aug Sept Oct / // / Nov Dec 50 ADULT (N=8264) 25 0 25 50 25 EGG 0 (N=642) 25 50 1ST 25 INSTAR 0 (N=2715) 25 50 2ND 25 INSTAR 0 (N=4249)25 50 3RD 25 INSTAR 0 (N=4290)25 50 4TH 25 INSTAR 0 (N=3061) 25 50 5TH 25 INSTAR 0 (N=3745) 25 50 Fig. 2. Composite field life cycle of B. hilaris on mesa pepperwort, London rocket, and broccoli in Las Cruces, NM, 2012–2014. Percentage in each sample of total individuals of the same stage. Percentages less than 5% may not be visible due to size of figure. Top horizontal bar represents actively growing periods of each host plant: gray ¼ mesa pepperwort; white diagonal stripes ¼ mesa pepperwort þ broccoli overlap; black diagonal stripes ¼ broccoli þ London rocket overlap; black ¼ London rocket þ mesa pepperwort overlap. 6 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA / / / / / Jan Feb Mar Apr May June July Aug Sept Oct Nov / / Dec 50 25 ADULT 0 (N=1884) 25 50 25 EGG 0 (N=50) 25 50 1ST 25 INSTAR 0 (N=136) 25 50 2ND 25 INSTAR 0 (N=922) 25 50 3RD 25 INSTAR 0 (N=992) 25 50 4TH 25 INSTAR 0 (N=1051)25 50 5TH 25 INSTAR 0 (N=1409)25 50 Fig. 3. Field life cycle of B. hilaris on London rocket and broccoli in Las Cruces, NM, 2012–2014. Percentage in each sample of total individuals of each stage. Percentages less than 5% may not be visible due to size of figure. Top horizontal bar represents actively growing periods of each host plant: gray ¼ broccoli; black diagonal stripes ¼ broccoli þ London rocket overlap; black ¼ London rocket; white ¼ neither host present. / / / / / Jan Feb Mar Apr May June July Aug Sept Oct Nov / / Dec 50 25 ADULT 0 (N=1884) 25 50 25 EGG 0 (N=50) 25 50 1ST 25 INSTAR 0 (N=136) 25 50 2ND 25 INSTAR 0 (N=922) 25 50 3RD 25 INSTAR 0 (N=992) 25 50 4TH 25 INSTAR 0 (N=1051)25 50 5TH 25 INSTAR 0 (N=1409)25 50 Fig. 4. Field life cycle of B. hilaris on London rocket and broccoli in Las Cruces, NM, 2012–2014. Percentage in each sample of total individuals of the same stage. Percentages less than 5% may not be visible due to size of figure. Top horizontal bar represents actively growing periods of each host plant: gray ¼ broccoli; black diagonal stripes ¼ broccoli þ London rocket overlap; black ¼ London rocket; white ¼ neither host present. 2015 TAYLOR ET AL.: LIFE HISTORY AND LABORATORY REARING OF B. hilaris Jan Feb Mar Apr May June July Aug Sept Oct 7 Nov Dec 50 25 ADULT 0 (N=6380) 25 50 25 EGG 0 (N=592)25 50 1ST 25 INSTAR 0 (N=2579)25 50 2ND 25 INSTAR 0 (N=3327)25 50 3RD 25 INSTAR 0 (N=3298)25 50 4TH 25 INSTAR 0 (N=2010)25 50 5TH 25 INSTAR 0 (N=2336)25 50 Fig. 5. Field life cycle of B. hilaris on mesa pepperwort in Las Cruces, NM, 2012–2014. Percentage in each sample of total individuals of each stage. Percentages less than 5% may not be visible due to size of figure. Jan Feb Mar Apr May June July Aug Sept Oct Nov Dec 50 ADULT (N=6380) 25 0 25 50 25 EGG 0 (N=592) 25 50 1ST 25 INSTAR 0 (N=2579) 25 50 2ND 25 INSTAR 0 (N=3327)25 50 3RD 25 INSTAR 0 (N=3298)25 50 4TH 25 INSTAR 0 (N=2010) 25 50 5TH 25 INSTAR 0 (N=2336) 25 50 Fig. 6. Field life cycle of B. hilaris on mesa pepperwort in Las Cruces, NM, 2012–2014. Percentage in each sample of total individuals of the same stage. Percentages less than 5% may not be visible due to size of figure. Eggs (n ¼ 642) were found from early February through early October (Figs. 1 and 2) and were deposited singly in the soil near the bases of sampled plants. Of these, 592 (92.21%) were collected from the bases of mesa pepperwort; the remainder was collected from the bases of London rocket and broccoli. Eggs never were collected on the host plants (Taylor et al. 2014). 8 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Table 2. Duration (in days) of immature stages of B. hilaris Stage Sex No. completing stadium Mean 6 SE Range Cumulative mean age 7.45 6 0.06 3.35 6 0.05 7.08 6 0.13 6.39 6 0.13 7.33 6 0.18 10.25 6 0.16 41.85 6 0.36 41.88 6 0.54 41.85 6 0.43 6–9 3–5 5–11 4–10 5–12 8–14 37–50 37–50 38–45 7.45 10.80 17.88 24.27 31.60 41.85 Males þ Females Males Females 100 91 84 76 73 68 68 40 28 a Egg First instar Second instar Third instar Fourth instar Fifth instar Egg through fifth instar a Of 2,866 eggs laid in the laboratory, 100 were selected for this study. The number of generations per year in this species was difficult to determine because of the multiple host plants, the extreme overlap of stadia, the variation in numbers per sample, and the absence of reproductive diapause (see above). All life stages, with the exception of the eggs, were present in every month of the year; eggs were not found in January, November, or December (Figs. 1 and 2). Adults and all nymphal instars overwintered (Figs. 1 and 2). Based on the seasonal abundance of the various life stages, the data roughly suggest that overwintering adults reproduced in late winter and spring and their offspring became adults in June–August (Figs. 1 and 2). The summer (second) generation reproduced primarily during July–September, and their offspring reached adults during September–November. These data suggest that this species is bivoltine. However, there is some evidence that there is a partial third generation in southern New Mexico, with overwintering late instars reaching adult in January and February (Figs. 1 and 2). Dividing the life cycle of B. hilaris into the time spent on London rocket (the winter annual) and broccoli, and the time spent on mesa pepperwort (the summer annual), further supports our contention that this species is bivoltine (Figs. 3–6). Specifically, adults and first through third instars were first collected on broccoli in early November, indicating original colonization likely occurred in October, and were found discontinuously into March when the plants senesced (Figs. 3 and 4). Adults and first through fifth instars first were observed on London rocket during early December and were found discontinuously into June (Figs. 3 and 4). Eggs were found discontinuously from February into May. Adults were found continuously throughout the year on mesa pepperwort, whereas the other life stages were found discontinuously (Figs. 5 and 6). However, all stages were most abundant from July through October (85.4% of total individuals collected; Fig. 6). Eggs were collected discontinuously from late February through mid-December; first instar nymphs from February into December; and second through fifth instars from early January discontinuously through December. Although the majority of the plants had senesced during the winter months, observations at this time showed that the bugs moved to the bases of the plants where some green leaves and debris remained and provided cover. Laboratory Rearing. Eggs (n ¼ 2,866) were laid in one of two general patterns: singly (n ¼ 2,760, 96.30%) or in groups, 2–11 eggs (n ¼ 106); those laid in a group were either deposited in a mass (n ¼ 38, 35.85%), or in a row (n ¼ 68, 64.15%). Eggs laid singly were deposited on the four available substrates: cheesecloth (n ¼ 1,891, 68.51%), paper toweling (n ¼ 653, 23.66%), cage surfaces (n ¼ 205, 7.43%), and plant material (n ¼ 117, 4.24%); eggs laid in groups were deposited on cheesecloth (n ¼ 36, 33.96%), paper toweling (n ¼ 35, 33.02%), cage surfaces (n ¼ 18, 16.98%), and plant material (n ¼ 17, 16.04%). Adults usually were found on the plant material. Egg color ranged from cream-colored to light brown when laid and changed to a dark pink color by day 5. Eyespots usually appeared at day 4, and the egg burster became visible by day 5. The incubation period ranged from 6–9 d and averaged 7.45 d (Table 2). The first instar emerged through the pseudopercular opening at the cephalic end of the egg with the aid of an egg burster. The first, second, third, fourth, and fifth stadia averaged 3.35, 7.08, 6.39, 7.33, and 10.25 d, respectively. Total development averaged 41.85 d and did not differ significantly between sexes (males, 41.88 d; females, 41.85 d; t ¼ 0.55; df ¼ 25; P ¼ 0.5890) (Table 2). Descriptions of Immature Stages Egg (Figs. 7–11). Length, 0.93 6 0.03 mm; width, 0.77 6 0.02 mm. Eggs typically laid singly in the soil (see Taylor et al. 2014) resulting in a layer of soil particles glued to the chorion (Fig. 7). Each egg subcylindrical, cream-colored to light brown; chorion spinose (Fig. 8); pseudoperculum present at cephalic end, convex and circular, surrounded by 11–18 micropylar processes (Figs. 8 and 9); processes clavate and recurved, smooth, 47.70 6 0.91 mm in length and 11.15 6 0.20 mm in diameter, opening subapical, 5.83 6 0.35 mm in diameter (Fig. 10); egg burster roughly T-shaped, heavily sclerotized, surrounded by membranous region, giving entire structure a subquadrate appearance (Fig. 11). Instars. The first instar is described in detail, but only significant changes from previous instars are described for subsequent instars. Length was measured from the apices of the tylus and juga to the apex of the abdomen (two measurements), width across the metanotum and abdominal segments 3 2015 TAYLOR ET AL.: LIFE HISTORY AND LABORATORY REARING OF B. hilaris 9 Fig. 9. Scanning electron micrograph of a B. hilaris egg (dorsal view), 130 . Fig. 7. Scanning electron micrograph of a B. hilaris egg extracted from soil but covered with adhering soil particles (lateral view), 100 . Fig. 8. Scanning electron micrograph of a B. hilaris egg recovered from cheese cloth (lateral view), 100 . Fig. 10. Scanning electron micrograph of micropylar process of B. hilaris, 1,200 . 10 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Fig. 11. Egg burster of B. hilaris. and 4 (two measurements). Additional measurements are given in Table 3. First Instar (Figs. 12 and 20). Length, 1.19 6 0.03 mm (1.20 6 0.03 mm); width, 0.71 6 0.02 mm (0.77 6 0.02 mm). Body elliptical; widest at abdominal segments 3–4; reddish, with head and thorax reddish brown. Head reddish brown, often with paired, faint brown longitudinal stripes adjacent to inner margin of eye, occasionally second faint pair from near base of tylus to near posterior margin of head, converging posteriorly; region posterior to eye and median oval area near posterior margin of head incompletely sclerotized; head strongly declivent; anterolateral margins generally straight, weakly arcuate near base of antenniferous tubercle; compound eyes oval, weakly pedunculate; tylus distinctly exceeding juga. Antennae foursegmented, often concolorous with head; apical segment longest, fusiform; ratio of antennal segment lengths 1:1.3:1.4:3. Labium four-segmented, generally concolorous with head. Thoracic nota reddish brown. Pro- and mesonota completely sclerotized, lateral margins weakly arcuate, posterior margins weakly arcuate medially, substraight laterally. Metanotum sclerotized in anterior two thirds, forming plate, this plate narrowed medially, posterior margins of plate and segment (i.e., membranous area) straight medially; mediolongitudinal line extending from anterior margin of pronotum through posterior margin of metanotal plate. Ratio of pro-, meso-, and metanotal lengths (sclerotized and membranous portion combined) 1:0.7:0.5. Pleura reddish brown; sterna reddish. Legs concolorous with body except for distal tip of tarsomere 2, which is dark brown. Abdomen, reddish dorsally, with six medial plates (plate 4 absent in first instar) and nine lateral plates, last medial (6) and last lateral (9) apparently fused and adjacent to sclerotized anal peritreme, which completely encircles anus; all plates reddish brown. Medial plate 1 subrectangular, plate 2 subquadrate, plate 3 suboval, plate 5 suboval, plate 6 arcuate; medial plates 1–3 with paired ostioles. Lateral plates extending dorsally and ventrally from lateral edge of abdomen: dorsally, plates 1–7 subtriangular to subquadrate; lateral plate 8 rounded; pseudointersegmental lines present mesad of lateral plates 1–7. Ventral surface mostly concolorous with corresponding dorsal surface; seven faint medial plates present: plates 1–3 paired, transverse, narrow; plates 4–7 subquadrate, plate 7 adjacent to anal peritreme; ventral extensions of lateral plates subquadrate. Abdominal spiracles on segments 2–6 each near lateral margin of corresponding segment. Single trichobothrium (primary trichobothrium) posteromesad of each spiracle on segments 3–7, arising from reddish brown sclerite. Second Instar (Figs. 13 and 21). Length, 1.50 6 0.05 mm (1.51 6 0.05 mm); width, 0.91 6 0.02 mm (1.14 6 0.04 mm). Head and thorax light brown. Head, dorsally, more completely sclerotized including region posterior to eye, median oval area near posterior margin of head completely sclerotized; longitudinal stripes darker; anterolateral margins of head slightly emarginate; paired incipient ocelli occasionally present posteromesad of compound eyes; eyes pedunculate; longitudinal groove present adjacent to base of antenniferous tubercle. Ratio of antennal segment lengths 1:1.8:1.9:3.3. Thorax, dorsally, with suture (pronotal suture) extending diagonally from anterolateral margin to approximately one half the length of pronotum. Proand mesonota with medial area weakly extended posteriorly, substraight laterally. Metanotal plate slightly more sclerotized medially. Ratio of pro-, meso-, and metanotal lengths 1:0.6:0.2. Ventral surface light brown. Legs with tarsomere 2 usually concolorous with other leg segments. Abdomen, dorsally, with paired, minute transverse sclerites along anterior margin of segment 1 midway between lateral margins and midline; medial and lateral plates darker; medial plate 4 consisting of paired sclerites; pair of faint white spots on second (and occasionally first) abdominal segment midway between lateral margins and midline. Ventrally, with medial plates well developed, plate 7 contiguous with lateral plate 9; a medial irregular sclerotized spot occasionally present between paired plate 3 and medial plate 4. Anal peritreme more heavily sclerotized, widest dorsally. Sclerite surrounding each primary trichobothrium larger. Second smaller trichobothrium (secondary trichobothrium) present on segments 3–7 adjacent to and slightly laterad of primary trichobothrium, incorporated into lateral abdominal plates. All plates from first instar larger. Otherwise, like first instar. Third Instar (Figs. 14–15, 22). Length, 2.30 6 0.04 mm (2.29 6 0.04 mm); width, 1.28 6 0.02 mm (1.62 6 0.03 mm). Two color forms present, one light (Figs. 14 and 22) and one dark (Fig. 15). Head, dorsally, with juga and portions of head adjacent to eyes occasionally cream-colored in light form, usually lacking in dark form. Tylus and juga subequal in length; paired incipient ocelli present posteromesad of compound eyes. Ratio of antennal segment lengths 1:2:1.9:2.9. Pronotum often with dark ringlike spot adjacent to pronotal suture. Mesonotum occasionally with paired 2015 TAYLOR ET AL.: LIFE HISTORY AND LABORATORY REARING OF B. hilaris 11 Table 3. Measurements (means 6 SE, mm) of B. hilaris instarsa Nymph b Body length (juga) Body length (tylus)c Head length (juga)d Head length (tylus)e Thorax widthf Abdomen width Width across eyes Synthlipsis Antennal segments First Second Third Fourth Beak segments First Second Third Fourth Notal lengthsg Pronotum Mesonotum Metanotum Leg lengths Protrochanter Profemur Protibia Protarsus Protarsomeresh First Second Mesotrochanter Mesofemur Mesotibia Mesotarsus Mesotarsomeresh First Second Metatrochanter Metafemur Metatibia Metatarsus Metatarsomeresh First Second First instar Second instar Third instar Fourth instar Fifth instar 1.19 6 0.03 1.20 6 0.03 0.44 6 0.01 0.47 6 0.01 0.71 6 0.02 0.77 6 0.02 0.53 6 0.01 0.39 6 0.01 1.50 6 0.05 1.51 6 0.05 0.47 6 0.01 0.49 6 0.01 0.91 6 0.02 1.14 6 0.04 0.66 6 0.01 0.50 6 0.02 2.30 6 0.04 2.29 6 0.04 0.65 6 0.01 0.66 6 0.01 1.28 6 0.02 1.62 6 0.03 0.86 6 0.03 0.55 6 0.06 3.22 6 0.05 3.16 6 0.05 0.87 6 0.02 0.88 6 0.02 1.92 6 0.06 2.29 6 0.07 1.26 6 0.01 0.85 6 0.01 4.62 6 0.21 4.55 6 0.21 1.04 6 0.04 0.99 6 0.04 2.61 6 0.08 3.04 6 0.13 1.64 6 0.03 1.05 6 0.03 0.09 6 0.01 0.12 6 0.01 0.13 6 0.01 0.27 6 0.01 0.11 6 0.01 0.20 6 0.01 0.21 6 0.01 0.36 6 0.01 0.16 6 0.00 0.32 6 0.00 0.31 6 0.01 0.46 6 0.01 0.24 6 0.01 0.55 6 0.01 0.48 6 0.01 0.58 6 0.01 0.27 6 0.01 0.88 6 0.02 0.68 6 0.01 0.76 6 0.01 0.12 6 0.00 0.15 6 0.00 0.09 6 0.01 0.17 6 0.00 0.17 6 0.00 0.26 6 0.01 0.12 6 0.00 0.20 6 0.00 0.25 6 0.00 0.41 6 0.00 0.17 6 0.01 0.26 6 0.00 0.34 6 0.01 0.58 6 0.01 0.22 6 0.01 0.34 6 0.01 0.46 6 0.02 0.78 6 0.01 0.31 6 0.01 0.44 6 0.01 0.15 6 0.01 0.11 6 0.00 0.08 6 0.01 0.22 6 0.00 0.14 6 0.01 0.04 6 0.00 0.35 6 0.01 0.27 6 0.01 0.05 6 0.02 0.57 6 0.01 0.53 6 0.01 0.14 6 0.00 0.86 6 0.02 1.01 6 0.04 0.08 6 0.01 0.12 6 0.01 0.25 6 0.01 0.28 6 0.01 0.22 6 0.01 0.18 6 0.01 0.33 6 0.01 0.42 6 0.01 0.27 6 0.00 0.25 6 0.01 0.50 6 0.01 0.60 6 0.03 0.37 6 0.01 0.34 6 0.01 0.74 6 0.01 0.91 6 0.01 0.51 6 0.01 0.45 6 0.02 1.12 6 0.03 1.29 6 0.04 0.76 6 0.02 0.07 6 0.00 0.17 6 0.00 0.12 6 0.01 0.27 6 0.01 0.31 6 0.01 0.22 6 0.00 0.10 6 0.00 0.20 6 0.01 0.17 6 0.01 0.40 6 0.01 0.46 6 0.01 0.28 6 0.01 0.16 6 0.01 0.25 6 0.01 0.26 6 0.00 0.63 6 0.02 0.68 6 0.01 0.38 6 0.01 0.23 6 0.01 0.35 6 0.00 0.34 6 0.01 0.92 6 0.02 1.01 6 0.01 0.53 6 0.01 0.39 6 0.01 0.46 6 0.02 0.47 6 0.01 1.32 6 0.03 1.41 6 0.04 0.79 6 0.01 0.08 6 0.01 0.17 6 0.00 0.13 6 0.00 0.30 6 0.01 0.35 6 0.01 0.23 6 0.01 0.11 6 0.00 0.20 6 0.00 0.18 6 0.00 0.45 6 0.01 0.57 6 0.01 0.30 6 0.01 0.17 6 0.01 0.27 6 0.00 0.26 6 0.00 0.71 6 0.02 0.88 6 0.01 0.41 6 0.01 0.24 6 0.01 0.35 6 0.01 0.36 6 0.00 1.05 6 0.02 1.33 6 0.02 0.53 6 0.02 0.41 6 0.01 0.46 6 0.02 0.46 6 0.02 1.56 6 0.05 1.91 6 0.07 0.85 6 0.01 0.08 6 0.00 0.17 6 0.00 0.12 6 0.00 0.21 6 0.00 0.18 6 0.01 0.29 6 0.00 0.26 6 0.02 0.38 6 0.01 0.44 6 0.01 0.49 6 0.02 a Measurements are based on 10 individuals per instar. Measured from tip of juga to apex of abdomen with head in normal declivent position. c Measured from tip of tylus to apex of abdomen with head in normal declivent position. d Measured from tip of juga to base of head in horizontal position. e Measured from tip of tylus to base of head in horizontal position. f Measured across metanotum. g Measured at midline. h Total length of segment measurements > overall length because of curvature. b dark transverse marks midway between lateral margins and mediolongitudinal line. Pro- and mesonota usually cream-colored medially in light form, pronotum creamcolored near lateral margins; pro- and mesonota usually without cream-colored markings in dark form. Pro- and mesonota with medial area more extended posteriorly, posterior margins rounded medially, straight laterally in pronotum, arcuate laterally in mesonotum; mediolongitudinal line usually extending from anterior margin of pronotum to posterior margin of mesonotum. Ratio of pro-, meso-, and metanotal lengths 1:0.8:0.1. Tibiae occasionally with cream-colored mediolongitudinal stripe in light form, absent in dark form. Abdomen, dorsally, with paired transverse sclerites of abdominal segment 1 larger; anterior margin of medial plate 1 often extended anteromedially, posterior margin often concave medially; anterior margin of medial plate 2 often convex medially; medial plate 3 subrectangular; medial plate 4 with paired sclerites fused, subrectangular. Paired white spots on abdominal segments 1 and 2 usually more pronounced; additional pair between medial plates 2 and 3. Cream-colored spot occasionally present on lateral plates in light form, never present in dark form. Ventrally, medial plate 7 and lateral plate 9 now fused; medial irregular sclerotized spot occasionally present between paired plates 2 12 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Fig. 12. Fig. 13. First instar of B. hilaris (dorsal view). Fig. 14. view). Third instar of B. hilaris, light form (dorsal Fig. 15. view). Third instar of B. hilaris, dark form (dorsal Second instar of B. hilaris (dorsal view). and 3; spot between paired plate 3 and medial plate 4 always present; all plates from second instar larger. Otherwise, like second instar. Fourth Instar (Figs. 16–17, 23). Length 3.22 6 0.05 mm (3.16 6 0.05 mm); width, 1.92 6 0.06 mm (2.29 6 0.07 mm). Two color forms present, one light (Figs. 16 and 23) and one dark (Fig. 17). Head with juga equal to or slightly exceeding length of tylus; paired ocelli more evident. Ratio of antennal segment lengths 1:2.3:2:2.4. Thorax with cream-colored markings now extending along lateral and anterior margins of pronotum in light form, occasionally with faint light spots on pro- and mesonota, mesad of pronotal suture; markings greatly reduced or absent in dark form, often present as narrow stripe parallel to lateral margin (Fig. 17). Lateral margins of pronotum substraight, those of mesonotum more strongly arcuate. Mesonotum with posterior margin rounded medially, strongly arcuate laterally; wing pads evident, extending to abdominal segment 2. Metanotal wing pads evident but not as well defined as anterior pair. Ratio of pro-, meso-, and metanotal lengths 1:0.9:0.2. Pleura often with creamcolored markings. Femora occasionally with faint 2015 Fig. 16. view). Fig. 17. view). TAYLOR ET AL.: LIFE HISTORY AND LABORATORY REARING OF B. hilaris 13 Fourth instar of B. hilaris, light form (dorsal Fig. 18. view). Fifth instar of B. hilaris, light form (dorsal Fig. 19. view). Fifth instar of B. hilaris, dark form (dorsal Fourth instar of B. hilaris, dark form (dorsal cream-colored mediolongitudinal stripe in light form, absent in dark form; tibiae often with cream-colored mediolongitudinal stripe in light form, absent in dark form. Abdomen, dorsally, with paired transverse sclerites of segment 1 larger; medial abdominal plates 1–4 more elongate transversely; anterior margin of medial plate 1 often produced laterally as irregular thin extension or as series of small sclerites; posterior margin of medial plate 1 slightly concave; anterior margin of medial plate 2 slightly convex; all plates from third instar larger. Additional pair of white spots present between medial plates 3 and 4. Cream-colored spot present on lateral abdominal plates in light form; absent in dark form. Otherwise, like third instar. Fifth Instar (Figs. 18–19, 24). Length 4.62 6 0.21 mm (4.55 6 0.21 mm); width, 2.61 6 0.08 mm (3.04 6 0.13 mm). Two color forms present, one light (Figs. 18 and 24) and one dark (Fig. 19). Cream-colored markings (now often tinged with yellow or orange) of head 14 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Figs. 20–24. Heads of B. hilaris (anterior view). (20) First instar. (21) Second instar. (22) Third instar, light form. (23) Fourth instar, light form. (24) Fifth instar, light form. extending to ocellus and, with slight break, to posterior margin of compound eye in light form; absent in dark form. Juga exceeding length of tylus. Ratio of antennal segment lengths 1:3.3:2.5:2.8. Thorax with cream-colored markings (now often tinged with yellow or orange) often extending twothirds the length of lateral margins of mesonotum in light form; light spots more evident on pro- and mesonota; all markings on pro- and mesonota, including those on lateral margins of mesonotum, greatly reduced or absent in dark form. Mesonotum with posterior margin more acute medially, more strongly arcuate laterally. Wing pads well developed; mesonotal pads extending to abdominal segments 3–4, metanotal pads same length. Ratio of pro-, meso-, and metanotal lengths 1:1.2:0.1. Femora often with cream-colored medial longitudinal stripe in light form, absent in dark form. Abdomen, dorsally, with transverse sclerites of segment 1 no longer visible; lateral extensions of medial plate 1 well developed; medial plate 5 and lateral plates 8 fused. All plates from fourth instar larger. Otherwise, like fourth instar. Diagnosis. The five instars are readily distinguishable by characters other than differences in body size. The first instar differs from later instars by the color of the head and thorax, which is reddish brown; presence of an incompletely sclerotized medial oval spot on the head; eye shape, which is weakly pedunculate; absence of a well-defined groove anterior to the eye; absence of a pair of thoracic sutures on pronotum; presence of five dorsal medial abdominal plates; and a single 2015 TAYLOR ET AL.: LIFE HISTORY AND LABORATORY REARING OF B. hilaris trichobothrium posteromesad of each spiracle on segments 3–7; older instars have a darker head and thorax, a completely sclerotized medial oval spot on the head, pedunculate eyes, a well-defined groove anterior to the eye; a pair of thoracic sutures on pronotum; six dorsal medial abdominal plates, and two trichobothria posteromesad of each spiracle on abdominals segments 3–7. The second instar can be distinguished from later instars by the lack of light and dark forms, the lack of cream-colored markings on the head and thorax, and the posterior margin of the mesonotum, which is substraight laterally; older instars have light and dark forms, light forms with cream colored markings on head and thorax and dark forms with markings absent or reduced; and the posterior margin of the mesonotum, which is arcuate laterally. The third instar lacks wing pads and can be distinguished from the fourth and fifth instars in which the wing pads are easily discernible. The fourth and fifth instars can be distinguished by the lengths of the wing pads, which reach abdominal segment 2 in the fourth instar and abdominal segments 3 or 4 in the fifth. Acknowledgments We thank the following individuals (all from New Mexico State University): undergraduate Danielle Lara and research associate Helen Vessels, for assistance in collection of field samples; arthropod museum curator, Graeme Davis, for assistance in imaging specimens for illustrations; Peter Cook for use of the scanning electron microscope; and Tessa Grasswitz for review of the manuscript. References Cited Ahuja, D., R. K. Kalyan, U. R. Ahuja, S. K. Singh, M. M. Sundria, and A. Dhandapani. 2008. Integrated management strategy for painted bug, Bagrada hilaris (Burm.) inflicting injury at seedling stage of mustard (Brassica juncea) in arid western Rajasthan. Pesticide Res. J. 20: 48–51. Arakelian, G. 2008–2009. Bagrada bug (Bagrada hilaris), pp. 25–26. In S. Gaimari and M. O’Donnell (eds.), California Plant Pest Dis. Rep. 25: 1-108. Atwal, A. S. 1959. 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