The genus Antiteuchus comprises 43 known species worldwide (Fernandes & Grazia 2006). Species in this genus are all phytophagous, feeding on the phloem of vascular plants (Grazia et al. 2015), such as annona, avocado, breadfruit, cacao, hibiscus, macadamia, and mango (Eberhard 1975; Umaña & Carballero 1995; Panizzi 1997; Ortega-León 2001; Villegas 2005). The biology and ecology of many of these species has never been studied in detail and information about host-plant records and damage are scarce. The species Antiteuchus innocens Engleman & Rolston (Hemiptera: Pentatomidae) is apparently of economic importance in avocado trees (Persea americana Miller) (Lauraceae) (Ortega-León 2001), and its presence has been reported in several countries of Central America, including Belize, Costa Rica, Guatemala, Honduras, and Mexico (Engleman & Rolston 1983; Ortega-León 2001; Grazia et al. 2015).

In the highlands of Chiapas, Mexico, A. innocens has been observed in high densities feeding on pines (Pinus sp.). Its presence has been related to the decline of forest plantations (CONAFOR 2014). Previous reports of phytophagous Hemiptera feeding on pines include Lygus lineolaris (Palisot de Beauvois) (Miridae), Gastrodess grossipes De Geer (Lygaeidae), Leptoglossus occidentalis Heidemann (Coreidae), Priapismus pini Rolston (Pentatomidae), and Antiteuchus rukesi Rolston (Pentatomidae) (Rolston 1991; Feci et al. 2003; Dixon & Fasulo 2015). Antiteuchus innocens is considered an emergent pest of pines in the highlands of Chiapas (CONAFOR 2014).

The purpose of this study was to determine the life cycle of A. innocens in pine ecosystems of Chiapas, Mexico. Observations on the biology and ecology of A. innocens will increase our knowledge of this species and assist in the development of pest management strategies.

Table 1.

Number of adults and immature stages of Antiteuchus innocens collected from pines during 2 yr in 3 localities of Chiapas, Mexico.

Materials and Methods

The study was conducted in the municipality of Altamirano, located in the central highlands of Chiapas. The climate in this area is semi-warm, wet, with rain almost uniformly distributed throughout the year (García 2004). There were 3 experimental sites: Paraje Chalota (16.725833°N, 92.030833°W, 1,264 masl); Pamala (16.883055°N, 91.998611°W, 1,267 masl), and Naranjo (16.715555°N, 92.037222°W, 1,298 masl). The region is important for conifer diversity, and the studied localities are naturally populated with Pinus oocarpa and P. maximinoi (both Pinaceae).

To determine the host-plant range of A. innocens, in each site we observed the different species of pines and surrounding vegetation to detect the presence or damage by A. innocens. In the case of pines, 10 P. oocarpa that exhibited damage by A. innocens (subapical part of the bud) were selected in each site. We took sample branches (40–50 cm long) that were cut with scissors and taken to the laboratory in plastic bags. Samples were taken every 3 wk during 2 yr (2012 and 2013). In the laboratory, samples were processed, and the developmental stages of A. innocens were identified by comparison with those described by Engleman & Rolston (1983), and Ortega-León (2001). We tabulated the frequency of biological stages of A. innocens collected over time, and with this information we obtained the life cycle of A. innocens. Specimens were preserved in vials with 70% ethanol.

Finally, 30 gravid females were collected in the field and taken to the laboratory. They were kept individually in 14.5 × 10.5 cm plastic containers and offered pieces (2–4 cm long) of P. oocarpa as oviposition substrate. The containers were maintained at 25 °C and a 12:12 h (L:D) photoperiod. The following variables were measured: number of egg masses per female, number of eggs, egg-hatching time, and development time from first to second instar. Pine branch tips were offered as food, and replaced when needed. Because the rearing of this insect beyond the second instar was unsuccessful, we used the insect stage frequencies of our field samplings to estimate the insect development through instars 2 to 5 following the Manly model (Manly 1974). This model assumes an insect population containing individuals developing through several stages, with a normal distribution for entry times to each biological stage, and a constant daily survival rate in all stages, which allows estimation of the duration of instars. The statistical analyses were performed using the R version 3.4.4 (R Development Core Team 2018).

Results

Adults and immature stages of A. innocens frequently were found in branches of the pines Pinus oocarpa, P. maximinoi, and P. devoniana (all Pinaceae). In total we collected 921 egg masses, 24,539 nymphs, and 3,064 adults, in a 2 yr period that correspond to 2 generations of A. innocens (Table 1). It was observed that the insect was more abundant in tall pines (> 5 m), and did not attack trees less than 3 m high. Even though we sampled other plants such as Myrica cerifera L. (Myricaceae), Eupatorium sp. (Asteraceae), Miconia argentea (Sw.) DC. (Melastomataceae), Psidium guajava L. (Myrtaceae), and Vernonia sp. (Asteraceae), among others, only pines were found to be damaged by A. innocens.

We determined that A. innocens has a univoltine life cycle. The life cycle from egg to adult was completed in about 310 d (Fig. 1). The juvenile development of this insect was: mean number of d (± SE): 8 (0.66), 8 (0.92), 41 (7.5), 79 (8.1), 122 (5.9), and 52 (6.9) d for egg incubation, and first, second, third, fourth, and fifth instar, respectively (Table 2). The sex ratio (males:females) was calculated to be 1.3:1.7. Longevity of adults was estimated to be about 54 d.

Adults of A. innocens do not exhibit sexual dimorphism. Generally, they gather in small groups up to 10 individuals in the subapical region of secondary branches of pines, and up to 20 individuals on the abaxial region of primary branches. They feed on pine needles in the subapical part of shoots (Fig. 2a). Copulation is typically undertaken at sunset (Fig. 2b), and can last several hours, sometimes until dawn. Adults disperse to other pines in short flights, generally late in the afternoon. Adults of A. innocens commonly gather in bark crevices of pines (Fig. 2d).

Fig. 1.

Typical life cycle (egg to adult) of the bug Antiteuchus innocens in the highlands of Chiapas, Mexico, showing the developmental stages and mean duration of each.

Table 2.

Analysis of stage frequency data from field samples to estimate the instar duration of the bug Antiteuchus innocens following the Manly model (Manly 1974).

Fig. 2.

Antiteuchus innocens on the pine Pinus oocarpa, in the highlands of Chiapas, Mexico: (a) adults feeding on needles, (b) adults mating, (c) female protecting eggs deposited on a female strobilus, (d) adults gathering on a stem crevice.

Females lay eggs at sunset, during the night or at an early hr in the morning. Egg masses are placed on abaxial stems of primary branches, on female strobili, and less frequently on small stems of secondary branches of pines. As with other species of hemipterans, eggs are barrel-shaped with a ring of small appendages. Initially they are white, changing to pink as incubation progresses. Females of A. innocens lay only a single mass of eggs, and abandon maternal care at the end of the first instar (Fig. 2c). Using their bodies, they protect egg masses to resist the attack of parasitoids and predators. The mean number (± SE) of eggs per mass was 28 (± 1), with 92.5% of eggs hatching.

Adults appeared in the field by Apr and reached their greatest abundance in May. Afterwards, adult abundance decreased gradually until Nov, when they were not recorded in the samples (Fig. 3). Oviposition occurred from Jun to Aug. After egg-hatching, the young nymphs remained clustered together near the remains of eggshells, and apparently do not feed during the first days of life. Instar I was detected in the field from Jun to Aug. Nymphs of instar II disperse from the oviposition sites (abaxial side of primary branches) to subapical parts of secondary branches of pines, presumably seeking food. Nymphs of instar II were present predominantly from Jun to Oct. From Oct onwards, most of the 5 instars of A. innocens were present in samples. Instars IV and V were more abundant in winter, during a period of 5 to 6 mo.

Discussion

This is the first study on the biology of A. innocens in pine ecosystems. This species is univoltine under the climatic conditions of Chiapas. Given that feeding of A. innocens was restricted to 3 species of pine, it was categorized as an oligophagous species. Previous reports mentioned avocado as a host of this bug (Ortega-León 2001; Saulich & Musolin 2014). However, our observations did not verify this fact and there are no reports of A. innocens feeding on avocado in Chiapas. Considering that most pentatomids are polyphagous (Panizzi 1997), the feeding of A. innocens on other species of plants in Chiapas cannot be discounted.

The reproduction of adults coincides with the hottest months of the year. Similar behavior also was observed with the bug Antiteuchus tripterus (Hemiptera: Pentatomdae) in Brazil (Panizzi & Grazia 2001). Oviposition by A. innocens females on the abaxial parts of primary branches may protect eggs from extreme abiotic factors, such as rain and sunlight. However, when pines produce female strobili (Jul and Aug), the bugs oviposit on it, perhaps because strobili are a rich source of nutrients that assures development of the progeny (Thompson & Pellmyr 1991). The maternal care exhibited by A. innocens is a common behavior of stink bugs belonging to subfamily Discocephalinae, and particularly for species of Antiteuchus (Eberhard 1975; Santos & Albuquerque 2001a, b; Taylor 1988). Maternal care in the genus Antiteuchus is more effective for predators than for parasitoids. However, it is also important to resist parasitoids, because to some degree it prevents egg parasitization by wasps of the genera Phanuropsis and Trissolcus (Hymenoptera: Platygastridae) (Eberhard 1975; Santos & Albuquerque 2001a; Matthews & Matthews 2010).

The longest period of development (> 4 mo) occurs in the fourth instar, possibly indicating the presence of diapause (Saulich & Musolin 2014). However, the presence of diapause was not verified, and the long developmental period is possibly due to the suboptimal climatic conditions, including reduction in photophase by about 2 h and decrease in temperature to about 9 °C in winter (Serrano et al. 2006). Even though members in the genus Antiteuchus are characterized by having long biological cycles that last several mo (and by its association with perennial plants), the life cycle of A. innocens was longer than those reported for other species. For instance, A. variolosus (Westwood) has a life cycle of 79 to 83 d at 22 °C (Barrera 1973); for A. tripterus (F.), it is 94 to 108 d at 24 °C (Umaña & Carballo 1995); and for A. sepulcralis (F.), it is 96 d at 25 °C (Santos & Albuquerque 2001). The long life cycle is one of the principal difficulties in establishing a laboratory colony of this species (Ortega-León 2001).

Fig. 3.

Relative frequencies per branch of the biological stages of Antiteuchus innocens collected on pine ecosystems of Chiapas, Mexico, during 2 consecutive yr.

Although our study was not designed to assess the level of damage by A. innocens to pines, it was clear that adults and nymphs attack pine cones for nourishment. Feeding on the cones can limit the proper growth of pines, and may cause damage to the plant, as mentioned for other species of bugs (Bates et al. 2000, 2002; Bracalini et al. 2013). Experiments designed to determine the economic injury level for this species should be performed in the near future.