BEHAVIOR
Unusual Ovipositional Behavior of the Stink Bug Bagrada hilaris (Hemiptera: Heteroptera: Pentatomidae) MELISE E. TAYLOR,1 C. S. BUNDY,1,2
AND
J. E. MCPHERSON3
Ann. Entomol. Soc. Am. 107(4): 872Ð877 (2014); DOI: http://dx.doi.org/10.1603/AN14029
ABSTRACT The stink bug Bagrada hilaris (Bermeister) (Hemiptera: Heteroptera: Pentatomidae) is an Old World pest recently established in North America. Literature on the ovipositional behavior of B. hilaris is limited. As part of a study on the seasonal biology of B. hilaris in New Mexico, we included observations of the odd egg-laying behavior of this bug. Here, we describe and illustrate the phases associated with this behavior. KEY WORDS Bagrada hilaris, Pentatomidae, ovipositional behavior, stink bug
The family Pentatomidae (stink bugs) contains ⬇4,700 species worldwide (Henry 2009). The life histories of several of these species have been documented, including reproductive behavior. As a general rule, these bugs deposit their barrel-shaped eggs in irregular round or hexagonal clusters or longitudinal rows on their host plants (Southwood 1956, Hinton 1981). All North American stink bugs apparently lay their eggs in this manner under normal conditions (e.g., Esselbaugh 1946, Hinton 1981, McPherson 1982, Javahery 1994), usually on leaves (McPherson and McPherson 2000). However, a few Old World pentatomids reportedly lay their eggs singly or in small clusters on detritus or on the soil surface (Puchkova 1961). The stink bug Bagrada hilaris (Burmeister) is an Old World pest of cole crops (Halbert and Eger 2010) found in Asia (including the subcontinent of India), Africa, the Middle East, and southern Europe (D. A. Rider, personal communication). This species was introduced into southern California in 2008 and has expanded its New World range from California east to New Mexico (Bundy et al. 2012) and Texas (Reed et al. 2013a) and north to Nevada (Perring et al. 2013). Literature on the ovipositional behavior of B. hilaris is limited. Eggs reportedly are laid singly or in clusters of 2 to 13 on the host plant (stems, leaves, inßorescences, or seed pods), detritus, or soil beneath the plants, or even in cracks in the soil (Pruthi 1946, Rakshpal 1950, Batra 1958, Ghosal et al. 2006, Arakelian 2010, Halbert and Eger 2010, Visser 2011, Perring et al. 2013, Reed et al. 2013b). Hinton (1981), in a key 1 Department of Entomology, Plant Pathology, and Weed Science, New Mexico State University, Las Cruces, NM 88003. 2 Corresponding author, e-mail:
[email protected]. 3 Department of Zoology, Southern Illinois University, Carbondale, IL 62901.
modiÞed from Puchkova (1961), reported that the related species Bagrada stolida (Herrich-Schaeffer) (as Bagrada stolata Horvath) deposits eggs singly or in clusters both on the host plant and in detritus around the plant. We are aware of only one report with direct Þeld observations of B. hilaris [as Bagrada picta (F.)] actually depositing eggs beneath the soil surface. Samuel (1949) reported that eggs were deposited ⬇1/4 inch (0.64 cm) below the surface in loose soil in “irregular groups of 15Ð75 eggs.” He further observed both Þrst instars of this bug and adult scelionid parasitoids later emerging from this spot. During a study of the life history of B. hilaris on Lepidium alyssoides A. Gray in southern New Mexico, we never recovered eggs from plant parts in the Þeld but did recover them from the soil (M.E.T., unpublished data). In the laboratory, one of us (C.S.B.) observed a female bug pushing her abdomen into the soil and moving in a way suggesting she was depositing an egg. Here, we document and describe the ovipositional behavior of this species. Materials and Methods An ovipositional arena (Fig. 1) was developed for laboratory observations to document the egg-laying behavior of B. hilaris. The bottom consisted of a small cookie sheet (35.0 cm in length by 23.5 cm in width by 1.5 cm in depth) Þlled with ⬇1 liter of Þeld soil; the soil was not homogenized (i.e., it contained various sizes of dirt clods scattered among Þne particles) to simulate Þeld conditions and to provide potential anchorage points for the bugs. Vertical sheets of white cardstock (21.6 by 27.9 cm) were cut into ⬇28 cm in length by 5 cm in width strips taped lengthwise along the perimeter of the sheet. The width of these strips was chosen because it provided a barrier to prevent escape
0013-8746/14/0872Ð0877$04.00/0 䉷 2014 Entomological Society of America
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Fig. 1. Arena for observing ovipositional behavior of B. hilaris. (Online Þgure in color.)
of the bugs and also provided access for videotaping. The arena was kept at room temperature (⬇22⬚C); sunlight from a nearby window was supplemented with a lamp (40 W) for optimal lighting for video recordings. A colony of Þeld-collected adult B. hilaris was maintained in the laboratory under controlled conditions (25⬚C ⫾ 0.01 and a photoperiod of 14:10 [L:D] h). One to Þve adult females were selected and placed in the arena after they had been observed initiating egglaying in the colony. Preovipositional and ovipositional behavior was videotaped for 24 females with a Sony CX380 digital video recorder attached to a tripod. Details of the ovipositional behavior were later reviewed and subdivided into phases. The length of each phase was determined using the internal time stamp provided by the recording device. A small disc of colored paper (each color corresponding to a speciÞc female) numbered in sequence was placed at each ovipositional site immediately after egg laying. After recording, the soil around each marker was collected, washed through a small hand-held strainer (80 mm in diameter) Þtted with mesh material (0.60 mm) to remove Þner particles. The eggs and courser particles remaining on the mesh were then washed into a petri dish and the eggs separated. For each female, notes were taken on the preovipositional and ovipositional periods, the number of eggs laid by a single female during oviposition, soil texture chosen, and anchoring behavior. The total time for each of the two periods and the time for the individual phases of oviposition were recorded. Because eggs were deposited beneath the soil, the exact moment of egg deposition could not be observed directly. Therefore, an additional series of videos (N ⫽ 40) were recorded for 12 females in which the ovipositional behavior was interrupted for each female at one of four points (beginning and middle of both the stationary and egg deposition phases, respectively; N ⫽ 10 for each point, using 3Ð 4 females per point)
during oviposition to determine speciÞcally when eggs were deposited (see Results and Discussion for description of phases). She was interrupted by gentle prodding with a paper disc held by forceps, which caused her to move immediately elsewhere; then, the disc was placed in the space previously occupied by the female. The soil around the disc later was removed (see paragraph above for details) and examined for eggs. Voucher Specimens. Selected samples of the bugs have been vouchered in the New Mexico State Arthropod Museum in Las Cruces, NM. Results and Discussion The 24 females selected for videotaping deposited 116 eggs. The video allowed us to identify six phases of behavior: phase 1, searching, which is preovipositional; and phases 2Ð 6, which are ovipositional (positioning, stationary, egg deposition, abdomen withdrawal, and egg covering) (see supp video [online only]). The time of each phase of behavior is summarized in Table 1. Searching Phase (Preovipositional Period). During this time, the female moved about the arena in search of a suitable place to deposit an egg. Most Table 1. Duration (in seconds) of the phases of ovipositional behavior of B. hilarisa Phaseb
Mean time ⫾ SE
Range
No. of observations
Positioning Stationary Egg deposition Covering Total event Intervalc
25.3 ⫾ 2.0 77.6 ⫾ 7.5 22.2 ⫾ 0.9 12.2 ⫾ 0.6 138.5 ⫾ 7.5 44.9 ⫾ 7.3
5Ð183 16Ð404 5Ð69 3Ð31 44Ð444 1Ð352
116 116 116 116 116 92
a
Based on 24 females. Abdomen withdrawal phase is not given here because its timing cannot be separated from the egg deposition and covering phases. c Time between ovipositions. b
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Fig. 2. Ovipositional behavior of B. hilaris, positioning phase. (A) Dorsal view. (B) Lateral view. 1) Body pivots left to right, 2) legs move forward and back for stability and aid in pushing abdomen below soil line, and 3) abdomen is pushed into soil. SC, clod of soil used as anchor point.
eggs (97 of 116; 85.8%) subsequently were deposited in Þne, loose soil that was not too shallow and provided good anchoring. The remaining eggs (N ⫽ 19) were deposited among small clods of soil (⬇1Ð10 mm in diameter). Positioning Phase (Beginning of Ovipositional Period). Once a suitable ovipositional site was reached, the female (typically) would anchor herself to the substrate on a dirt clod or soil particles using her pro- and mesothoracic legs (Fig. 2A). She then would pivot back and forth, pushing her abdomen into the soil (⬇0.5Ð2.0 mm in depth) (Fig. 2B). This was assisted with movement of her metathoracic legs and, when not anchored, her mesothoracic legs. Anchoring was observed in 95.7% of ovipositional events (111 of 116). This phase averaged 25.3 s (range, 5Ð183 s). Stationary Phase. The female ceased all external movement (Fig. 3). We believe this is when the egg
was passing through the oviduct in preparation for deposition. This phase averaged 77.6 s (range, 16 Ð 404 s). Egg Deposition Phase. The female became active again; her abdomen began to pivot back and forth (Fig. 4), and an egg was deposited in the soil (Fig. 5). This phase averaged 22.2 s (range, 5Ð 69 s). Abdomen Withdrawal Phase. As the female continued to pivot (Fig. 6A), she withdrew her abdomen from the soil (Fig. 6B). Covering Phase. As the female withdrew her abdomen from the soil, she moved her metathoracic legs beneath her abdomen, pushing dirt over the exposed egg (Fig. 7). However, the movement of her legs varied during this phase (N ⫽ 114). Generally, she alternated movement of her legs (left, right, left, etc.; N ⫽ 65); occasionally, she moved both legs together (N ⫽ 31); rarely, one leg covered the egg while the other was anchored to the soil (N ⫽ 18; Note: the
Fig. 3. Ovipositional behavior of B. hilaris, stationary phase. (A) Dorsal view. (B) Lateral view. Female ceases movement; apex of abdomen now below surface.
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Fig. 4. Ovipositional behavior of B. hilaris, egg deposition phase, part 1 (dorsal view). Body pivots side to side.
Fig. 5. Ovipositional behavior of B. hilaris, egg deposition phase, part 2 (dorsal view). Egg is deposited.
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Fig. 6. Ovipositional behavior of B. hilaris, abdomen withdrawal and covering phases (lateral view). (A) Body is withdrawn from soil. (B) Exposed egg before it was covered.
pattern of leg movement was not clearly visible on two occasions). Clear ßuid occasionally was observed (N ⫽ 12) being expelled from her abdomen at the end of this phase, before her moving to a new oviposition spot. This phase averaged 12.2 s (range, 3Ð31 s). The total ovipositional period from the positioning phase through covering of the egg averaged 138.5 s (range, 44 Ð 444 s). The average interval between ovipositions was 44.9 s (range, 1Ð352 s). Rarely (N ⫽ 9), the female began the ovipositional behavior (positioning phase) again in the same location immediately after covering the previous egg. A single egg was recovered from each completed oviposition (N ⫽ 116). On 12 occasions, however, the egg, rather than remaining in the soil, stuck to the femaleÕs abdomen after oviposition and eventually fell off, landing on the surface of the arena. This may explain previous reports of eggs deposited on the soil surface. Support for determining the actual time of egg deposition comes from the interruption videos (N ⫽ 40, 10 for each point; see Materials and Methods). The females were interrupted at one of the four points in the ovipositional process: 1) beginning of the station-
ary phase, 2) middle of the stationary phase (23Ð90 s after the phase began), 3) beginning of the egg deposition phase, or 4) middle of the egg deposition phase (3Ð22 s after the phase began). Eggs were not recovered from females interrupted at the beginning or middle of the stationary phase or during the beginning of the egg deposition phase (points 1Ð3, respectively). A single female had deposited an egg by the middle of the egg deposition phase (point 4); the remaining females (N ⫽ 9) each laid an egg immediately after point 4. Therefore, the majority of eggs was laid between the middle of the egg deposition phase and the beginning of the abdomen withdrawal phase. To our knowledge, this is the Þrst report of eggcovering behavior observed in a stink bug. Our data conÞrm the observations of Samuel (1949), who reported Þrst instars and parasitoids emerging from soil in India. Given the general trend among the Pentatomidae to deposit eggs in clusters on plant tissue, the behavior observed here is rare and may suggest some sort of selective pressure on the bugs in the region in which they evolved.
Fig. 7. Ovipositional behavior of B. hilaris, covering phase. (A) Dorsal view. (B) Lateral view. Metathoracic legs move back and forth under abdomen, covering egg with soil.
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TAYLOR ET AL.: UNUSUAL OVIPOSITIONAL BEHAVIOR OF B. hilaris Acknowledgments
We thank the following individuals from New Mexico State University: Danielle J. Lara, undergraduate, and Helen K. Vessels, research associate, for assistance in recording preovipositional and ovipositional behavior; and Juan E. Robles, videographer, for assistance in editing the ovipositional video. This research was partially funded by the New Mexico State Agricultural Experiment Station, Las Cruces, NM.
References Cited Arakelian, G. 2010. Bagrada bug. Center for Invasive Species Research. (http://cisr.ucr.edu/bagrada_bug.html) (accessed 10 January 2014). Batra, H. N. 1958. Bionomics of Bagrada cruciferarum Kirkaldy (Heteroptera: Pentatomidae) and its occurrence as a pest of mustard seeds. Indian J. Entomol. 20: 130 Ð135. Bundy, C. S., T. R. Grasswitz, and C. Sutherland. 2012. First report of the invasive stink bug Bagrada hilaris (Burmeister) (Heteroptera: Pentatomidae) from New Mexico, with notes on its biology. Southwest. Entomol. 37: 411Ð 414. Esselbaugh, C. O. 1946. A study of the eggs of the Pentatomidae (Hemiptera). Ann. Entomol. Soc. Am. 34: 667Ð 691. Ghosal, T. K., J. Ghosh, S. K. Senapati, and D. C. Deb. 2006. Biology, seasonal incidence and impact of some insecticides on painted bug, Bagrada hilaris (Burm.). J. Appl. Zool. Res. 17: 9 Ð12. Halbert, S. E., and J. E. Eger. 2010. Bagrada bug (Bagrada hilaris) (Hemiptera: Pentatomidae) an exotic pest of Cruciferae established in the western USA. Pest Alert, Fl. Dep. Agric. Consumer Services, Division of Plant Industry. (http://www.freshfromßorida.com/pi/pest-alerts/ pdf/bagrada-bug-pest-alert.pdf) (accessed 10 January 2014). Henry, T. J. 2009. Biodiversity of the Heteroptera, pp. 223Ð 263. In R. G. Foottit and P. H. Adler (eds.), Insect biodiversity: science and society. Wiley-Blackwell, Oxford, England. Hinton, H. E. 1981. Biology of insect eggs, v. 2. Pergamon, New York, NY. Javahery, M. 1994. Development of eggs in some true bugs (Hemiptera-Heteroptera). Part I. Pentatomoidea. Can. Entomol. 126: 401Ð 433.
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McPherson, J. E. 1982. The Pentatomoidea (Hemiptera) of northeastern North America with emphasis on the fauna of Illinois. Southern Illinois University Press, Carbondale and Edwardsville. McPherson, J. E., and R. M. McPherson. 2000. Stink bugs of economic importance in America north of Mexico. CRC, Boca Raton, FL. Perring, T. M., D. A. Reed, J. C. Palumbo, T. Grasswitz, C. S. Bundy, W. Jones, and T. Royer. 2013. National pest alert: bagrada bug Bagrada hilaris (Burmeister) Family Pentatomidae. U.S. Dep. Agric.-NIFA Regional IPM Centers. (http://www.ncipmc.org/alerts/bagradabug.pdf) (accessed 10 January 2014). Pruthi, H. S. 1946. Report of the imperial entomologist. Sci. Rep. Imperial Agric. Res. Inst., New Delhi, 1941. 44: 64 Ð 71. Puchkova, L. V. 1961. The eggs of Hemiptera-Heteroptera: VI. Pentatomoidea, 2, Pentatomidae and Plataspidae. Entomol. Rev. 40: 63Ð 69. Rakshpal, R. 1950. Notes on the biology of Bagrada cruciferarum Kirk. Indian J. Entomol. 11: 11Ð16. Reed, D. A., J. C. Palumbo, T. M. Perring, and C. May. 2013a. Bagrada hilaris (Hemiptera: Pentatomidae), An invasive stink bug attacking cole crops in the southwestern United States. J. Integr. Pest Manage. 4: 1Ð7. Reed, D. A., J. P. Newman, T. M. Perring, J. A. Bethke, and J. N. Kabashima. 2013b. Management of the bagrada bug in nurseries. Univ. California Coop. Ext., Agric. Nat. Resources, Ventura County. (http://ceventura.ucdavis. edu/Þles/163391.pdf) (accessed 9 May 2014). Samuel, K. C. 1949. Biological notes on two new egg-parasites of Bagrada picta Fabr (sic) Pentatomidae. Indian J. Entomol. 4: 92Ð93. Southwood, T.R.E. 1956. The structure of the eggs of the terrestrial Heteroptera and its relationship to the classiÞcation of the group. Trans. R. Entomol. Soc. Lond. 108: 163Ð221. Visser, D. 2011. The bagrada bugÐa secondary yet potentially destructive potato pest. CHIPS (Nov./Dec.): 30 Ð32. (http://www.potatoes.co.za/SiteResources/documents/ The%20Bagrada%20bug%202011.pdf) (accessed 9 May 2014). Received 14 February 2014; accepted 12 May 2014.
