Collection and Maintenance Rearing

The eggs of P. torridus collected in the field were placed in plastic boxes (Gerbox®) and kept in rooms with the temperature controlled to obtain the nymphs. After hatching, the nymphs were placed in cages for nymphal development. The insects collected in the field were identified by comparing them to samples from the Entomology Museum of the Entomology Laboratory of Embrapa Clima Temperado.

We collected insects at different developmental stages from experimental crops of jatropha of Embrapa Clima Temperado. The insects were kept in plastic tubes (10 × 15 × 10 cm) and transported to the laboratory, where they were placed in wooden cages (27 × 27 × 35 cm), with the sides covered with a nylon screen. In each cage, we placed 100 insects at ratio of 1 female for 1 male. For rearing, the insects were separated in cages prepared for the nymphal and adult stages. The nymphs and the adults were fed with branches, leaves and fruits of jatropha and aroeira [Schinus terebinthifolius Raddi (Anacardiaceae)]. The branches and leaves were placed in plastic pots (250 mL) with water to keep the plants turgid and the fruits were offered in Petri dishes (8.5 × 1.5 cm). The foods were replaced each four days. Inside the cages, we also placed a Petri dish (8.5 × 1.5 cm) with hydrophilic cotton embedded with water. In the cage for the adult stage, the branches and leaves were also the substrate for oviposition and the egg collections were carried out daily. After hatching, the nymphs were kept in cages especially designed for insects reared in laboratory.

Biology in Different Hosts

Adult Longevity and Reproduction

We isolated randomly 20 pairs of adult insects, newly emerged from nymphs fed with strawberry guava and jatropha in cages of plastic cups (700 mL). The open part of the cup was covered with a Gerbox® lid, and holes were made on it, then, covered with voile fabric for aeration. The adults were separated by sex according to their genital segments. Females show only genital plates, while the males have a developed pygophore at the rear of the abdomen.

The adults were fed with the same food used in the nymphal stage, offered in Petri dishes (8.5 ×l.5 cm). In each cage, we placed a plastic receptacle (3.5 cm wide × 1.5 cm high) containing cotton embedded in water. In addition, in each cage, we offered a branch with leaves of the respective hosts, in a 10-mL receptacle containing water, to serve as the substrate for oviposition. We carried out daily observations to register the number of eggs and adult mortality. We assessed the following biological parameters: pre-oviposition, oviposition, post-oviposition periods; fecundity; number of eggs in each oviposition; egg laying and life span of males and females. The survival and embryo period duration were determined based on the number of eggs laid in the second laying. For that purpose, the eggs and females were placed in a receptacle (22.5 × 15.0 × 11.5 cm) and kept in room with temperature controlled until the hatching of the nymphs.

Statistical Analysis

The experiment was carried out in a completely randomized design with 3 treatments (hosts) and 10 repetitions (hatched nymphs of 10 events of egg laying) for the nymphal stage and 20 repetitions (pairs) for adults. The data were subjected to analysis of variance and the means compared in the Student's t test, protected by the significance of the F test at 5% probability using the SAS program (SAS Institute 2002). The data regarding the periods of pre-oviposition, oviposition and post-oviposition and male and female longevity were analyzed using the survival analysis techniques (Colosimo & Giolo 2006). For each period, the survival curves of each treatment were estimated in the Kaplan-Meier estimator and compared in the log-rank test (Colosimo & Giolo 2006).

Development of the Nymphal Stage

The fruits of strawberry guava and jatropha allowed nymphal development of P. torridus, nymphs, but when reared on tung fruit, virtually 100% of the nymphs died as 2nd instars (Table 1). For the insects fed with strawberry guava and jatropha fruits, we observed 5 instars different only at the 5th instar, where the nymphal stadium lasted 6 days when reared jatropha than on strawberry guava (Table 1). However, the duration of the P. torridus nymphal stage whether fed on jatropha or on strawberry guava did not differ significantly, having a duration of 55.0 days when fed strawberry guava and 56.1 days when fed with jatropha (Table 1).

The shorter developmental period of the 1st instar in relation to the others is a characteristic of the Hemiptera (Brailovsky et al. 1992). Possibly due to the fact that this instar does not feed, and this occurs to other species of the super-family Pentatomoidea (Eberhard 1975; Peredo 2002). The 1st instars of species in this super-family probably use only reserves from the embryonic stage.

TABLE 1.

DURATION (DAYS) AND SURVIVAL RATE (%) (MEAN ± STANDARD ERROR) OF EACH INSTAR AND THE NYMPHAL STAGE OF PACHYCORIS TORRIDUS FED EITHER WITH STRAWBERRY GUAVA, JATROPHA OR TUNG AT 25 ± 2 °C, 70 ± 10% RH AND 12:12 H L:D.

Rodrigues et al. (2011) reported that at 24 ± 1 °C and 12:12 h L:D, P. torridus reared on jatropha fruits also had 5 instars with durations of 8.1, 10.0, 9.7, 11.6 and 11.7 days, respectively, totaling 52 days for nymphal development; which is, therefore, slightly shorter than the duration found in our study in which the temperature was 1 degree lower.

For nymphal development from the 1st to the 2nd instar, we observed a survival rate of 100% in the three treatments (Table 1). According to Panizzi and Silva (2009), the 1^st instar nymphs still do not have the buccal system and intestinal flora completely developed, and therefore, they do not feed, but use body reserves to reach the next stage, so that they require only humidity. First instar nymphs continue under oviposition, protected by the mother, who provides maternal care until the 2nd instar, second instars display gregarious behavior as they search for food. Similar behavior was observed for other species of Scutelleridae Pachycoris klugii Burmeister, 1835 and Pachycoris stallii Uhler, 1863 (Peredo 2002; Williams III et al. 2005).

The greater reduction of the survival rate in the nymphal stages was observed in the 2nd instar, which was significantly higher for nymphs fed with jatropha (Table 1). For the other instars, the survival rate remained above 75% (Table 1). Although occurrences of damage to the tung cultures caused by P. torridus have been reported (Nava et al. 2009), in our study, we observed that the early developmental stage of this stinkbug does not develop on this fruit, i.e., from the 2nd instar onwards, mortality is almost complete (Table 1). This shows that the attack behavior is different and, possibly, adults of the insect inflict damage to tung cultures. Possibly, the mortality for the 2nd instar of P. torridus on tung fruits is attributed to physical characteristics of the fruit's epicarp that has a fibrous texture (approximately 50.6%) (Gengling 2001) and, therefore, the nymphs would have more difficulty to drill through these tissues. Different results were observed for jatropha and strawberry guava, which have fleshy fruits and, thus, more suitable for the nymphs to feed on. Moreover, this hypothesis may be confirmed by the presence of only adults on the plants, which theoretically have better capacity to suck and feed.

The total survival rate of the nymphal stage was 35.7% for insects fed strawberry guava and 38.9% for those fed jatropha, and these rates were not significantly different (Table 1). Although considered low, these survival rates are higher than those reported by Rodrigues et al. (2011), who found 18.43% of survival rate for nymphs of P. torridus fed jatropha. This difference is probably attributed to the method used for the nymphal development, given that Rodrigues et al. (2011) reared insects in different cages and did not specify the number of insects used in each unit.

The sex ratio was not influenced by the food ingested in the nymphal stage, being 0.6 and 0.5 for insects fed with fruits of strawberry guava and jatropha, respectively. Therefore, we found a sex ratio of 1 female to 1 male, which is similar to populations studied in the field (Nava et al. 2009).

Adult Longevity and Reproduction

The weight of adults differed significantly when the insects were fed with different foods and between the sexes (Fig. 1). Females and males reared on fruits of jatropha (152.0 and 117.2 mg, respectively) were heavier than those reared on strawberry guava fruit (127.9 and 105.9 mg, respectively). Regarding the sexes, females reared on strawberry guava and jatropha (127.9 and 152.0 mg, respectively) were heavier than males (105.9 and 117.2 mg, respectively). The greater weight of insects reared on jatropha as compared to those reared on strawberry guava may be related to the nutritional aspect of the host. Possibly, jatropha contains the quantity and quality of nutrients required for the development of P. torridus. Therefore, the parameters of reproduction and longevity of P. torridus reared on jatropha reflect the insect development during the nymphal stage. The fact that the females may feed more in the adult stage, the formation of the reproduction system, and subsequent egg production occurs during the nymphal development (Panizzi & Silva 2009). Even though there are no studies comparing the development of P. torridus on different foods, this pest is of great importance to jatropha culture, and is considered a key pest of this culture (Carvalho et al. 2009).

Fig. 1.

Weights (mg) (means ± standard error) of females and males of Pachycoris torridus, determined 24 h after emergence, when fed with strawberry guava and jatropha at 25 ± 2 °C, 70 ± 10% RH and 12:12 h L:D. Means followed by the same letter (lowercase between sexes and uppercase between foods) do not differ in the Student's t test protected at significance of F test at 5% probability (gl = 316, F = 53.65, P < 0.00001).

Fig. 2.

Survival curve for the periods of pre-oviposition (A), oviposition (B) and post-ovipodition (C) for Pachycoris torridus reared on strawberry guava (Psidium cattleianum) and jatropha (Jatropha curcas) at 25 ± 2 °C, 70 ± 10% RH and 12:12 h L:D. Curves identified with the same letter do not significantly differ from one another. MST = Mean Survival Time.

The pre-oviposition period for females fed jatropha (134.9 days) was almost double the period found for strawberry guava (74.0 days) (Fig. 2A). The oviposition period for females fed strawberry guava (46.7 days) was roughly the double of the period for females reared on jatropha (22.6 days) (Fig. 2B). During the oviposition period, females fed with strawberry guava had 1.65 egg-laying events on average, amounting to an average of 59.15 eggs per female and 37.05 eggs per oviposition, while females fed with jatropha had 1.15 egg-laying events on average, roughly 42.3 eggs per female and 36.21 eggs per oviposition, and these differences were slight (Table 2). However oviposition when fed jatropha showed a greater number of eggs, ranging from 57 to 87 (Gabriel et al. 1988; Rodrigues et al. 2011).

The average number of eggs per oviposition was also lower than that collected from insects in the field, such as P. klugii and P. stallii, with values of 82.3 and 53.8 eggs per oviposition, respectively (Peredo 2002; Williams III et al. 2005). It is possible that in the field, insects have a greater variety of foods, mainly in the adult stage (Silva et al. 1968; Sanchez-Soto & Nakano 2002) and are, therefore, capable of supplying their nutritional requirements more adequately. Moreover, the developmental stage of fruits of jatropha and strawberry guava may also interfere diminish insect fecundity. According to Rodrigues et al. (2011), although P. torridus develops in seeds of jatropha, this insect shows preference for developing fruits, which possibly have a different physical and chemical constitution.

The duration of the post-oviposition period was 3 times longer for insects fed strawberry guava (68.9 days) than for those fed jatropha (20.7 days) (Fig. 2C).

Life span of adult insects fed jatropha was greater than that for adults fed strawberry guava (Fig. 3A and B). The same behavior was observed for males, while for females, there was no significant difference (Fig. 3C and D. In strawberry guava fruits, we also observed significant difference between males and females, while in jatropha fruits, although females lived longer, the difference was no significant. Rodrigues et al. (2011) reported life span of 93 days, therefore, shorter than the results in our study. The difference of approximately 50 days between the result obtained in the current study and those reported in the literature may also be related to the method used in the evaluation of longevity, given that Rodrigues et al. (2011) assessed adult longevity from nymphs collected in the field, while in our study, the insects used came from laboratory rearing. Moreover, the populations of P. torridus used are from different locations with distinct climatic conditions. Rodrigues et al. (2011) used populations from the Central-Western region in Brazil, which is characterized by tropical climate, while in our study; we used a population collected from the Southern region in Brazil, characterized by temperate climate. For the egg stage, we observed that the duration was roughly 11 days for both treatments. For the survival in the embryonic stage, eggs laid by females fed with jatropha had a survival rate (51.5%) significantly higher than for those fed with strawberry guava (32.1%) (Table 2). These values of the embryonic stage are similar to those found by Rodrigues et al. (2011) (12.7 days), while the survival rate for eggs reported by the authors was 90.5%. In case of embryonic period survival, probably the used method influenced on the study whether in this work the eggs under female care were removed from the laying place, while Rodrigues et al. (2011) didn't use this procedure.

TABLE 2.

MEAN VALUES (± STANDARD ERROR) OF BIOLOGICAL PARAMETERS OF PACHYCORIS TORRIDUS REARED ON STRAWBERRY GUAVA AND JATROPHA AT 25 ± 2 °C, 70 ± 10% RH AND 12:12 H L:D.

Thus, the fruits of strawberry guava and jatropha are adequate for the development and reproduction of P. torridus, however, this stinkbug shows greater weights for males and females and longer life span when fed with jatropha. Therefore, the management of this insect pest in jatropha cultivations should take into account the control of this pest in other hosts as well, such as strawberry guava, for the climatic conditions found in the Rio Grande do Sul State, Brazil. Given that the development of P. torridus occurred in jatropha and strawberry guava, the control should be applied soon after the occurrence of the pest in the culture to avoid its migration to others.

Fig. 3.

Survival curves for Pachycoris torridus. Graphs A refer to longevity of females reared on strawberry guava (Psidium cattleianum) and jatropha (Jatropha curcas); graph B refer to longevity of males reared on P. cattleianum and J. curcas; graphs C refer to longevity of females e males reared on P. cattleianum; and graphs D refer to longevity of females e males reared on J. curcas. 25 ± 2 °C, 70 ± 10% RH and 12:12 h L:D. Curves identified with the same letter do not significantly differ from one another. MST = Mean Survival Time.