Description.

Eggs cylindrical with convex ends. Length, 1.46 ± 0.13 (1.20-1.69, n = 101); width, 0.87±0.06 (0.71-1.02, n=101). Chorion with hexagonal reticulations surrounding smaller irregular sculpturing (Fig. 2). Cephalic pole with a ring of unevenly spaced micropylar processes, 19± 2.08 (14-23, n = 66). Pseudoperculum circular, sometimes askew, ovate; egg burster dark brown, subtriangular, T-shaped. Chorion relatively thin, weak, and pliable, similar to that of the pentatomid Euschistus servus (Say). Egg masses consisted of 53.8 ± 8.86 (33-74, n =40) eggs laid in roughly hexagonal groups. The average number of rows per egg mass was 8.47 ± 0.97 (6-11, n = 30). Egg masses averaged 6.80 ± 0.63 (5.43 - 8.23, n=39) in length and 5.95 ± 0.55 (4.75-7.20, n = 39) in width.

Leaves with egg masses averaged 35.0 ± 7.2 in length, and 13.0 ± 4.2 (n = 35) in width. The position of egg masses on leaves corresponded to the approximate center of the leaf (92% of maximum width, 44% of maximum length measured from leaf base). Egg masses usually overlapped the midvein, but occasionally were positioned entirely between the leaf margin and midvein. The longitudinal axes of eggs were not perpendicular to the leaf surface, but instead were always oriented toward the leaf base, (i.e., upward) at an angle. This angle of deviation from a line perpendicular to the leaf surface was 15.9° ± 12.4 (5-45, n=125). To our knowledge, this is the first recorded observation of this phenomenon in Pentatomoidea. Its function, if any, is unknown. Dimensions of egg masses were considerably less than those of adult females (egg masses: 6.80 x 5.95mm; adult females: 11.73 x 7.83 mm), thus egg masses were completely covered by the brooding females. The longitudinal axis of an egg mass was usually parallel to that of the leaf.Eberhard (1975) also reported this egg mass orientation for the pentatomid Antiteuchus tripterus limbativentris Ruckes and suggested that it might be due to the consistent position of the defending bug in relation to the orientation of the egg mass, as influenced by selection pressure of parasitic wasps.

Immediately after oviposition, eggs were cream-colored. As embryonic development proceeded, the embryos acquired a concolorous pigmentation of pale pink except for a cream-colored band extending from the caudal to cephalicregion. With further development, the eggs became pinkish orange, noticeable first in the eyes, clypeus, pronotum, and appendages. Finally, about 4 days after oviposition the embryos transformed to salmon, then darkened to red prior to eclosion. Hatching was observed on two occasions, both in the morning (28 July 1994, 0741-0751h, 34°C, two separate egg masses). When embryonic cuticles were recovered (n=83), they were matted together either on the portion of the egg mass nearest the leaf tip, or occasionally on the leaf just distal to this portion of the egg mass. Some of the eggs failed to develop (≤10%), and these undeveloped eggs remained creamy yellow. Color changes observed during development of P. stallii eggs were similar to those reported for other Pachycoris species (Hussey, 1934; Grimmetal., 1998; Peredo, 2002). Most P. stallii egg masses were parasitized by a wasp, Telenomus pachycoris (Costa Lima) (Hymenoptera: Scelionidae); parasitism rates averaged about 47% (Fig. 3). Parasitized eggs turned from gray to black as the parasitoids developed. Antagonism by ants, Dorymyrmex bicolor Wheeler (Hymenoptera: Formicidae), sometimes caused brooding P. stallii females to abandon their egg masses, after which the ants devoured the eggs (Fig. 4).

Lockwood and Story (1986a) postulated that nonrandom embryonic orientation, i.e., dorsoventral polarity, of prolarvae is an adaptive function that reduces mortality of first instars. We assessed the embryonic orientation for P. stallii prolarvae within egg masses that were not parasitized by T. pachycoris. These unparasitized egg masses were similar to those described previously, consisting of 55.4 ± 11.06 (34-73, n = 14) eggs. Embryonic orientation in these egg masses was not related to position of egg with in the mass. Instead, each embryo was oriented with its venter directed down (i.e., toward the ground) regardless of the location of the egg within the mass. Other studies also reported uniform embryonic orientation in scutellerids. Javahery (1994) reported that eggs of Eurygaster alternata (Say), E. integriceps Puton, and E. maura (L.)were oriented in one direction, as did Reid and Barton (1989) for Chelysomidea guttata (Herrich-Schaeffer). However, neither study indicated the direction of the embryos. Eberhard (1975) found that embryos of the pentatomid A. t. limbativentris were all oriented in the same direction in each egg mass, although neither the direction of embryos in an egg mass nor differences in embryonic orientation between egg masses were reported. However, embryonic orientation of other pentatomid species was dependent on egg location with in the mass, as influenced by form of egg mass, number of eggs, and number of rows in an egg mass, and could be described as a ‘center orientation’ for emerging nymphs(Lockwoodetal., 1986a; Javahery, 1994). Lockwood and Story (1986a) demonstrated that embryonic orientation in Nezara viridula (L.) varied with egg position within the mass, was extrinsically mediated, and facilitated formation of first-instar aggregations. This ‘center orientation’ of embryos enhanced survival and development of N. viridula (Lockwood etal., 1986b), and may serve a similar function in other pentatomoids. Although the embryonic orientation of P. stallii differed from that described for most pentatomoids, it may nevertheless provide an adaptive function. The uniform downward embryonic orientation of P. stallii may facilitate formation of first-instar aggregations at a relatively safe location on the leaf (i.e., between the egg mass and the distal tip of the leaf). This would position the brooding female bug between the nymphs and the only route by which crawling natural enemies could gain access to the leaf. Thus, the mother would be in a position to defend her offspring.

First Instar

(Fig. 5a). Color as for fifth instar, without metallic green. General color red. Legs pale brown, tinged with red. Eyes red. Total length,2.57 ± 0.05 (2.50-2.60). Length of head, 0.62 ± 0.02 (0.60-0.63); width of head, 0.88 ± 0.01 (0.87-0.90). Width of eye, 0.12 ± 0.01 (0.12 - 0.13); interocular space, 0.64 ± 0.01 (0.63 - 0.65). Rostral length, 1.17 ± 0.07 (1.08 - 1.25). Antennal length, 1.11 ± 0.05 (1.03-1.15); ratio of segment lengths about 1:1.78:1.64:3.43. Length of pronotum, 0.25 ± 0.01 (0.24-0.25); width of pronotum, 1.09 ± 0.04 (1.03-1.13). Abdominal length, 1.41 ± 0.04 (1.37-1.47); abdominal width 1.66 ± 0.06 (1.60-1.73).

Second Instar

(Fig. 5b). Color as for fifth instar, without metallic green. Legs dark brown. Abdomen red. Eyes red. Total length, 3.27 ± 0.09 (3.20-3.40). Length of head, 0.78 ± 0.02 (0.75-0.80); width of head, 1.19 ± 0.03 (1.15-1.22). Width of eye, 0.19 ± 0.01 (0.18-0.20); interocular space, 0.81 ± 0.02 (0.78-0.83). Rostral length, 2.14 ± 0.1 (2.00-2.22); ratio of segment lengths about 1:2:1.34:1.29. Antennal length, 1.75 ± 0.05 (1.70-1.82); ratio of segment lengths about 1:1.65:1.5:2.58. Length of pronotum, 0.38 ± 0.01 (0.37-0.40); width of pronotum, 1.50 ± 0.06 (1.42-1.57). Abdominal length, 1.65 ± 0.08 (1.57-1.75); abdominal width, 2.10 ± 0.12 (2.00-2.27).

Third Instar

(Fig. 5c). Color as for fifth instar, without metallic green. Eyes dark red. Abdomen red. Total length, 4.29 ± 0.1 (4.18-4.43). Length of head, 0.94 ± 0.13 (0.75-1.17); width of head, 1.69 ± 0.04 (1.63-1.75). Width of eye, 0.29 ± 0.02 (0.27-0.32); interocular space, 1.11 ± 0.04 (1.05-1.17). Rostral length, 2.93 ± 0.07 (2.89-3.05); ratio of segment lengths about 1:2.11:1.21:1.31. Antennal length, 2.65 ± 0.04 (2.64-2.75); ratio of segment lengths about 1:2.15:2.03:2.85. Length of pronotum, 0.62 ± 0.03 (0.58-0.65); width of pronotum, 2.28 ± 0.16 (2.08-2.51). Abdominal length, 2.34±0.37 (1.98-2.81); abdominal width, 2.87±0.36(2.48-3.35). Stridulitrum on venter of abdomen consisting of a series of coarse fingerprint-like elongate ridges on sternites 5, 6, and anterior portion of 7, less pronounced than in fourth instar.

Fourth Instar

(Fig. 5d). Eyes dark red. Total length, 5.23 ± 0.21 (4.94-5.38). Length of head, 0.98 ±0.17 (0.83-1.24); width of head, 2.27 ± 0.03 (2.23-2.30). Width of eye, 0.39 ± 0.01 (0.30-0.40); interocular space, 1.48 ± 0.02 (1.45-1.50). Rostral length, 3.32 ± 0.02 (3.30-3.35); ratio of segment lengths about 1:2:1.19:1.25. Antennal length, 3.64 ± 0.04 (3.60-3.69); ratio of segment lengths about 1:1.92:1.86:2.37. Length of pronotum, 0.97 ±0.05 (0.90-1.00); width of pronotum, 3.82 ± 0.08 (3.74-3.94). Wing pad length, 1.22 ± 0.06 (1.15-1.30). Abdominal length, 2.76 ± 0.21 (2.53-3.04); abdominal width, 4.28 ± 0.17 (4.05-4.43). Stridulitrum on venter of abdomen consisting of a series of coarse fingerprint-like elongate ridges on sternites 5, 6, and anterior portion of 7, less pronounced than in fifth instar.

Fifth Instar

(Fig. 5e). Total length, 6.77 ± 0.46 (6.33-7.41). Length of head, 1.01 ± 0.30 (0.63-1.37); width of head, 2.91 ± 0.09 (2.79-3.00). Body broadly oval; shiny, coarsely punctate. Head dark brown, almost black, with a metallic green sheen; laterally dark brown except under the eyes, brown. Bucculae pale brown. Clypeus not surpassing the jugae, with short, sparse setae. Eyes prominent, rounded from lateral view, nearly contiguous with pronotum. Eyes dark red. Width of eye, 0.56 ± 0.02 (0.53-0.58); interocular space, 1.90 ± 0.05 (1.83-1.93). Rostrum dark brown. Rostral length, 4.46 ± 0.02 (4.57-4.60); ratio of segment lengths about 1:1.79:0.96:1.2. Antennae dark brown, almost black, union between segments pale brown; short abundant setae. Antennal length, 5.31 ± 0.09 (5.20-5.40); ratio of segment lengths about 1:2.41:2.18:2.22.

Abdominal length, 3.58 ± 0.08 (3.48-3.67); abdominal width, 5.57 ± 0.23 (5.38-5.89). Abdomen pale brown medially, laterally tinged with orange, rugose; dark brown, almost black with metallic green plates. Ventrally brown, medially pale brown, rugose; laterally tinged with orange, dark brown plates (Fig. 5f); sparsely setose. Paired ostia of dorsal abdominal scent glands located between terga 3 and 4, 4 and 5, and 5 and 6, with reticulate microsculpturing near ostiole and occlusion arm (see Williams et al. 2001). Using the criteria of Remold (1962), ostioles of the anterior dorsal abdominal glands of type 1 (undivided ostiole), while median and posterior ostioles intermediate between types 1 and 2 (divided ostiole). Stridulitrum on venter of abdomen consisting of a series of coarse fingerprint-like elongate ridges on sternites 5, 6, and anterior portion of 7 (Fig. 6a, b). Ventral surface of metathoracic tibia with ridges with ca. 20 small tubercules (Fig. 6c, d).

Thorax with three distinct segments. Pronotum dark brown, almost black, with metallic green sheen, except edges brown tinged with orange, flat laterally; punctate. Length of pronotum, 1.60 ± 0.14 (1.43-1.77); width of pronotum, 5.55±0.12 (5.38-5.63). Meso-and meta sternum brown. Wing pad length, 2.98±0.04 (2.93-3.03); dark brown, almost black, with metallic green sheen. Ventrally pale brown, tinged with orange. Legs dark brown, almost black; sparsely setose. Tarsi with pulvilli and parempodia as seen in Figure 6e.

Dimensions of P. stallii nymphs were similar to thoseof P. klugii studied in México (Peredo, 2002), although P. stallii had a slightly shorter antenna, rostrum, and head. Fourth- and fifth-instar P. stallii had smaller bodies overall (i.e., length and width) than P. klugii (Peredo, 2002). Dimensions of P. klugii nymphs studied in Nicaragua (Grimmet al., 1998) were considerably larger than P. stallii. As with eggs, these differences may be proportional to adult body size.

Life History and Development of Nymphs. All nymphal instars, as well as adults and eggs, were found throughout the year; thus, P. stallii appears to be bi-or multivoltine. After eclosion, first instars remained aggregated on or near the egg mass from which they hatched, and were guarded by the mother (Fig. 7). These nymphs were relatively inactive and were usually in contact with one another and sometimes the mother. Aggregation of first instars with the attending mother is consistent with other species of Pachycoris (Hussey, 1934; Grimm et al., 1998; Peredo, 2002). Female bugs brooding eggs were never observed feeding. First-instar P. stallii also appeared to abstain from feeding, as do first instars of many other Pentatomoidea (Walt et al., 1972; Eberhard, 1975; Oetting et al., 1975; Peredo, 2002).

The effect of maternal brooding behavior on survival of first-instar nymphs was evaluated by experimental removal of female bugs guarding nymphs that had just emerged. Our results indicated that brooding of first instars significantly increased their survival (P<0.05) (Fig. 8). Removal of guarding female bugs resulted in a rapid increase in nymphal mortality, reaching 100% after 4 days. Mortality of untreated controls was less than 4% at the end of the 6-day study. Behavior of first instars in the absence of the guarding adult was noticeably different from nymphs that were guarded. Unguarded nymphs often separated into two or three groups within a day after removal of the guarding female, and dispersed to other parts of the plant, often the apex of stems. Although predation of nymphs was not observed during the study, it is possible that disruption of nymphal aggregations predisposes nymphs to greater predation. However, Grimmand Somarriba (Grimm et al., 1998) found that first-instar P. klugii reared in outdoor cages that excluded most if not all predators also suffered 100% mortality when abandoned by the mother.Antiteuchus t. limbativentris first instars suffered substantial losses (≥40%) when guarding mothers were experimentally removed (Eberhard, 1975). Results of these studies indicate that the presence of the brooding mother plays a critical role in the aggregative behavior of nymphs and their subsequent survival. The mechanism is unknown, but it is possible that brooding Pachycoris females provide a cue, chemical and/or physical, that is necessary for the stability of nymphal aggregations. Our results suggest that maternal guarding behavior is a net benefit to P. stallii. Possible costs to the brooding female, such as starvation and increased risk from natural enemies, await further study. Eberhard (1975) also showed that the net effect of maternal guarding of first-instar A. t. limbativentris was positive.

Second-instar nymphs remained aggregated, but did not remain near the brooding female. We did not observe separation of these nymphs and the adult, but P. klugii nymphs moved away from the mother after molting to second instar (Peredo, 2002). However, Eberhard (1975) reported the reverse situation for A. t. limbativentris; mothers abandoned their second-instar offspring. Aggregations of second-instar P. stallii were most commonly observed feeding on C. californicus fruit (Fig. 9a) or resting on leaves (Fig. 9b). They were much more active than first instars and readily crawled away when disturbed. Third through fifth instars were also very active, and exhibited similar feeding and resting behavior (Fig. 10) as second instars. However, aggregations of third through fifth instars consisted of progressively fewer individuals with age, so that fifth instars were usually solitary. This may be a resul tof cumulative nymphal mortality and/or normal decay of aggregative behavior. In contrast to what we observed, Grimm and Somarriba (Grimm et al., 1998) found that aggregations of P. klugii nymphs remained intact until after adult metamorphosis. Moltingin P. stallii was observed on two occasions (28 July 1994, 0701 hours, 31° C, emergence of a fourth instar; 19 January 1997, 1353 hours, 27°C, a callow fourth instar on leaf in shade 7.5 cm above soil). On 28 December 1990, 1200-1415 hours the behavior of nymphs and adults was observed during a light/moderate rain. These condition shad no apparent effect on the behavior of P. stallii ; bugs were active feeding and resting as usual. During the summer months nymphs were generally observed either resting in shaded portions of the plant canopy, or if in direct sunlight, were nearly always feeding on fruit or occasionally on the stem.

Pachycoris stallii nymphs are subject to biotic and abiotic mortality factors. Predation on P. stallii nymphs was rarely observed. Adult female Zelus sulcicollis Champion (Heteroptera: Reduviidae) were observed feeding on third-instar nymphs on two occasions (15 April 1990, 1500-1530 hours; 1 November 1995, 1515 hours in the plant canopy about 3 cm above soil surface). Ants, Dorymyrmex bicolor, were sometimes observed attacking nymphs on the soil beneath C. californicus. When leaves harboring nymphs were placed on the sand indirect sunlight the nymphs crawled to and froon the leaf and within 5 minall had fallen or crawled off the leaf on to the sand; within 2 min they became immobilized by the heat and after an additional 2 min they died. Within 30 min they were found by D. bicolor. These observations indicate that typical surface temperatures during summer days are lethalto P. stallii nymphs that fall from plants, and thus interplant dispersal by nymphs is unlikely. However, it is possible that nymphs could survive surface temperatures during summer nights or during other seasons when temperatures are more moderate, although interplant dispersal via the ground might still expose them to greater risk of predation. These limits to nymphal dispersal suggest that nymphs usually mature to adulthood on their natal host plant. Clearly, muchre mains to be learned about the biology of P. stallii. Future studies will address P. stallii -natural enemy associations, and the effect of environmental factors on the life history of this bug.