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CHEMISTRY and DEFENSIVE EFFICACY of SECRETION of BURROWING BUG (Sehirus Cinctus Cinctus)

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CHEMISTRY and DEFENSIVE EFFICACY of SECRETION of BURROWING BUG (Sehirus Cinctus Cinctus) Journal ofChemical Ecology. Vol. 23. No.8. 1997 7821 CHEMISTRY AND DEFENSIVE EFFICACY OF SECRETION OF BURROWING BUG (Sehirus cinctus cinctus) BRYAN S. KRALL,I.* BRUCE W. ZILKOWSKI,2 SCOTT L. KIGHT,3 ROBERT J. BARTELT,2 and DOUGLAS W. WHITMAN! '4120 Biological Sciences. J//inois State University Normal. J//inois 61790 1USDA. ARS Narional Center for Agricultural Utilization Research Bioactive Agents Research Unit 1815 N. University. Peoria. J//inois 61604 3Depanment ofBiology and Center for the Integrative Study ofAnimal Behavior Indiana University Bloomington. Indiana 47405 (Received September 16, 1996; accepted April 2, 1997) Abstract-Adult Sehirus cinctus cinctus emit a volatile secretion from their metathoracic scent glands when tactually stimulated. We identified the volatile components by gas chromatography, high-performance liquid chromatogra­ phy. and mass spectrometry. The secretion of both sexes contained (lR)-(+)­ a-pinene. (lS)-( - )-,B-pinene, ,B-myrcene, (R)-( + )-limonene, and a-terpino­ lene. Two additional compounds were found in only female secretions: (E)-2-hexenyl acetate and (E)-2-octenal. We also tested the defensive capa­ bility of this insect by offering it to various predators. Anoles, starlings, and a killdeer rejected S. c. cinctus after an initial sampling. These findings sug­ gest that the secretion plays a defensive role. Key Words-Terpenes, chemical defense, Heteroptera, Cydnidae, Sehirus cinctus cinctus. (IR)-( + loa-pinene, (IS)-( - )-,B-pinene. ,B-myrcene, (R)-( +)­ limonene. a-terpinolene. (E)-2-hexenyl acetate, (E)-2-octenal. INTRODUCTION Hemipterans are well known for their use of repellent chemicals to defend themselves against predators (Staddon, 1979; Blum, 1981; Aldrich, 1988). *To whom correspondence should be addressed. 1951 0098.()33119710800-1951SI2.5010 @ 1997 Plenum Publishing Corporation 1952 KRALL ET AL. However, not much is known about the defensive chemistry of cydnids, a cos­ mopolitan family closely related to the Pentatomidae (Miller, 1971). Even less is known about chemical defense in the cydnid subfamily Sehirinae. In the United States, the Sehirinae are represented by one genus containing one species and three subspecies. The most common subspecies, Sehirus cinctus cinctus (Palisot de Beauvois), ranges from Massachusetts to Florida and as far west and south as Iowa, New Mexico, and Mexico (Froeschner, 1960). Cydnids in general, and S. c. cinctus in particular, are unique in that they practice brood care in underground chambers (Sites and McPherson, 1982). Adult S. c. cinctus overwinter and emerge in late March to April to feed in aggregations on several species of mint. By the end of April, adults mate and move to the ground (Sites and McPherson, 1982), where the females find or 3 dig a small (ca. 0.5 cm ) chamber approximately 2 cm below the soil surface and lay a batch of 120-150 eggs. Females remain with the eggs and early-instar larvae for several weeks, guarding them against ants and other predators and feeding them by carrying mint seeds from the surface'to the chamber (Southwood and Hine, 1950; McDonald, 1968). The nymphs leave the brood chamber when they reach the third instar and travel to the surface to feed on mint foliage (Sites and McPherson, 1982). They pass through five instars before reaching adulthood and can be found between early May and mid-August, while adults can be found from early Spring to late Summer. S. c. cinctus nymphs are aposematically colored. They are black with reddish orange markings on the head, thorax, and abdomen. Adults may also be aposematic when viewed against green vegetation. They are small (ca. 5 mm long), black insects with a thin cream-colored stripe along the lateral margins of each wing beginning at the head and extending down to the anterior of the wings. When stimulated by lightly pinching the legs or antennae, the adults emit a volatile secretion. This suggests that the secretion functions in chemical defense against predators. METHODS AND MATERlALS Insect Collection and Care Adult S. c. cinctus were collected on wild mints near Bloomington, Indiana, in early April 1995. The bugs were then kept in a cold chamber for three months at 7°C under a lOL: 14D photoperiod to preserve them until needed. After retrieval from the cold chamber, individuals were maintained according to Sites and McPherson (1982) with the following modifications: no plastic wrap was placed over the Petri dish, as this induced harmfully high humidities. Instead, a l-cm2 screened ventilation hole was placed in the center of each plastic Petri BURROWING BUG SECRETIONS 1953 dish lid. Vial caps containing dried fruits ofPrunella vulgaris (Labiatae) allowed the bugs to feed ad libitum. Chemical Analysis Chemicals. (1S)-( - )-a-Pinene (98%), dl-a-pinene (99%), (1R)-( +)-{3­ pinene (98 %), (1S)-( - )-{3-pinene (99 %), (R)-( +)-limonene (97 %), (S)-( -)­ limonene (96%), a-terpinolene (99%), and (E)-2-octenal (94%) were purchased from Aldrich Chemical Co., Milwaukee, Wisconsin. J3-Myrcene (90%) and (E)-2-hexenyl acetate (97 %) were obtained from Sigma Chemical Co., St. Louis, Missouri. Volatile Collection and Analysis. The sex of ca. 25 S. c. cinctus adults was detennined using a microscope, and the insects were placed individually into Hewlett-Packard autosampler vials (glass, 12 mm x 32 rom, with an II-rom Teflon-lined aluminum crimp cap). A 500-Jotl gas-tight syringe was used to draw 200 Jotl of headspace volatiles out of each vial. Volatiles were then immediately injected into a GC for analysis (Hewlett-Packard 5890, equipped with splitless injector, and flame ionization detector). The DB-l capillary column (J &W Scientific, Folsom, California) was 15 m x 0.25 rom and had a 1.0-Jotm film thickness. The temperature program was 50-150°C at lOoC/min. Following analysis of the first gas sample, the cap was removed from the vial, and the insect was agitated by either grabbing a leg with forceps or holding the individual against the sides or bottom of the vial until the characteristic odor was obvious to the investigator. (In some cases merely attempting to grab an insect without actually restraining it was enough to elicit release of the secretion). At the first hint of chemical release, a new cap was tightly crimped on to the vial and a second headspace volatile sample (200 Jot!) was removed and injected into the GC. A second method of volatile collection was used for ca. 50 unsexed dead adult S. c. cinctus. Dead adults (deceased adults stored at -SoC within 24 hr of death and kept up to one month before extraction) were covered with 5 rnl of hexane and then crushed with a glass rod. The sample was filtered, reduced in volume under Nz, and then fractionated isocratically with high-perfonnance liquid chromatography (HPLC) using a Waters Associates 6000 pump and a Waters Associates R401 refractometer detector. A silica column (Lichrosorb Si60, 25 cm x 0.46 cm, 5-Jotm particle size) was eluted with hexane (flow 1 rnI/min) and effluent was collected as consecutive l-rnl fractions. These frac­ tions were analyzed by GC. The fractions provided a larger amount of material than from single headspace collections, making it possible to obtain mass spectra for the insect-derived compounds and to determine chirality for some com­ pounds. Mass spectra were obtained on a Hewlett-Packard 5970 MSD instru­ ment, with sample introduction through a DB-l capillary column (15 m x 0.25 1954 KRALLETAL. mm ID with 1.0-lLm film thickness, temperature program 50-250°C increased at lOoC/min). Chirality was detennined on a chiral GC column by comparison to authentic standards. A 30-m x 0.25-mm-ID CDX-B fused silica capillary column (J & W Scientific) with a 0.25-lLm film thickness was used (temperature program 40-75°C at lOoC/min, then holding at 75°C for 30 min). Seed Extraction. Prunella vulgaris seeds were cleaned of debris and 0.5 g was placed into a glass vial with 2 ml of hexane; the seeds were crushed with a glass rod. The extract was filtered and analyzed by GC (Hewlett-Packard 5890, 15-m x 0.25-mm-ID DB-I capillary column with 0.25-lLm film thickness, temperature program 50-250°C increased at lOoC/min). Predator Trials Anolis carolensis carolensis. Six adult anole lizards, obtained from a local pet shop, were maintained for two weeks at 2rC with surplus food (various arthropods) and water. The anoles were isolated and starved for two days prior to testing. Each anole was tested individually in its home container by gently introducing a series of adult S. c. cinctus. Houseflies (Musca domestica) and small, second- to fourth-instar Acheta domesticus crickets served as control prey. To begin each test, an anole was initially offered a control insect to verify hunger. Next, S. c. cinctus adults were sequentially offered until the anole refused to attack them. This two-step process was repeated until the anole con­ tinually rejected S. c. cinctus, yet continually ate controls. This process was repeated two or three days later. Onychomys leucogaster. Two laboratory-reared northern grasshopper mice were obtained from the Animal Care Facility at illinois State University. Mice were starved for 4 hr prior to testing and were tested in their home containers. Third- and fourth-instar A. domesticus crickets were used as controls. Each mouse was offered a control cricket followed by five S. c. cinctus in sequence. Charadrius vociferus. A l-week-old killdeer was reared in the lab on a diet of arthropodS, earthwonns, snails, fish and fruit. At about 4 weeks of age, when the bird could feed by itself and discriminate among prey (i.e., began to prefer some prey items over others), it was tested in the following method: The bird was given a control third-instar A.
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