The cowpea, (Vigna unguiculata [L.] Walp) (Fabaceae), is a legume that originated in Africa and India (Phillips et al. 2003; Freire Filho et al. 2005). This agronomic crop is among the most economically important food sources produced in the tropical and subtropical regions of the world. In Brazil, cowpeas are traditionally grown in the northern portion of the country. However, production of this legume is rapidly spreading into the northeastern and central-western Cerrado regions, either as a primary crop or a late harvest after soybeans or rice (Ribeiro 2002; Freire Filho 2011).

Several insect pests feed on cowpea causing significant damage at different phenological stages of the plant. Some phytophagous hemipterans, e.g., Crinocerus sanctus (F.), Piezodorus guildinii (Westwood), and Nezara viridula (L.) (Coreidae and Pentatomidae) attack V. unguiculata at the flowering and grain ripening stage (Ribeiro 2002; Silva et al. 2005). All these species damage cowpea in a similar way by feeding on buds, new leaves, and pods causing deformities that can reduce the size and yield of grains. Moreover, Ribeiro (2002) reported that hemipteran pests can inject toxins directly into the plants, further reducing productivity of the crop (Ribeiro 2002).

Generally, Pentatomidae are widely distributed throughout most of Brazil, where 605 species have been described (Grazia & Fernandes 2012; Panizzi & Grazia 2015), but little is known about this fauna in the northeastern part of the country. Distribution records for some genera are limited to single studies or species of agricultural importance. However, Firmino et al. (2017) recently conducted a study in fragments of the tropical Atlantic Forest in northeastern Brazil and found that the richness of the Pentatomidae species in this ecosystem was comparable with those from subtropical southern Brazil.

The family Coreidae includes several polyphagous species that feed on monocotyledons and dicotyledons, although more commonly associated with the latter. In the Neotropics, the most common species of coreids are C. sanctus, Anisoscelis foliacea (F.), Holhymenia histrio (F.), Leptoglossus gonagra (F.), Leptoglossus zonatus (Dallas), Phthia picta (Drury), Anasa tristis (De Geer), and Spartocera dentiventris Berg (Panizzi & Grazia 2015). Information on the distribution of Coreidae on agronomic plants in Brazil is very limited. Only 2 species of coreids have been associated with cowpea: L. zonatus and C. sanctus. Crinocerus sanctus is a pest of this crop in northeastern Brazil, causing reductions in yield by feeding during pod formation that adversely affects seed filling. Because this feeding damage considerably affects grain quality and production, this species has been designated as a primary economic pest of this crop (Silva et al. 2005).

Many microhymenopteran species attack the eggs of phytophagous hemipterans that could be important natural biocontrol agents against these pests. Moreover, several parasitoid species in this order have been observed by some workers to be responsible for maintaining populations of these pests below economically damaging levels (Corrêa-Ferreira 1986; Pacheco et al. 1999). In Brazil, 23 species of microhymenopterans have been reported as egg parasites of hemipteran pests of soybean, the most commonly cited ones being Telenomus podisi (Ashmead) and Trissolcus basalis (Wollaston) (Hymenoptera: Platygastridae) (Loiácono 1980; Corrêa-Ferreira & Moscardi 1995; Loiácono & Margaría 2002). Studies on egg parasitoids are critical for identifying possible agents for use in biological control programs, particularly identifying those that impact agricultural pests in the local fauna because parasitoid-host diversity varies among crop systems and geographic regions.

The fauna of Coreidae and Pentatomidae on cowpea in Brazil is little known. Because of the recent expansion of cowpea production into the cerrado (savannah) areas of the country, it is critical that identification of phytophagous hemipterans on this crop be conducted, including any associated egg parasitoids. Therefore, we conducted a study to measure the diversity and composition of phytophagous Coreidae and Pentatomidae, as well as their egg parasitoids on cowpea in dry and rainy seasons in northeastern Brazil.

Materials and Methods

Results

POPULATION FLUCTUATIONS AND SEASONALITY

There were major differences in the richness and diversity indices of hemipteran species between the 2 seasons (Table 2). During the rainy season, the predominant species in collections were: C. ubica, C. sanctus, E. heros, and P. guildinii. During the dry season, only 3 very abundant species were found, i.e., P. guildinii, E. tragulus, and H. fulvus, although P. guildinii was collected more frequently than the other species during this time (Table 1). Hemipteran abundance was negatively correlated with temperature (r = −0.47; P < 0.05), weakly negatively correlated with precipitation (r = −0.05; P > 0.5), and positively correlated with humidity (r = 0.43; P < 0.05).

Table 1.

Species, abundance, and relative frequency of Pentatomidae and Coreidae from sweep net collections on cowpea in Teresina, Piauí, Brazil, 2015.

The most favorable climate factors for an increase in hemipteran populations, i.e., higher humidity and lower temperatures, occurred during the rainy season. Conversely, hemipteran population growth was hindered under extreme conditions of the dry season, due to high temperatures, low humidity, and near-zero precipitation (Fig. 3).

Discussion

Our results showed that hemipteran species richness on cowpeas in northeastern Brazil was greater than other studies conducted in similar agronomic growing regions of the country. We collected a total of 14 species of Pentatomidae from 3 subfamilies and 5 species of Coreidae from the subfamily Coreinae. In a previous population survey conducted by Fazolin (1995) on cowpea crops (in the city of Rio Branco, state of Acre, Brazil), 4 species of Pentatomidae were found, namely Euschistus sp., Oebalus poecilus (Dallas), O. ypsilongriseus (De Geer), and P. guildinii, as well as 2 species of Coreidae, C. sanctus and L. zonatus. That study also observed higher abundance of Euschistus sp., P. guildinii, and C. sanctus in their collections for this crop, just as we observed in our study. In addition, Marsaro Junior and Pereira (2013) assessed population fluctuations of the main pests of cowpea in the state of Roraima during the months of Aug to Oct 2006 (using a beating cloth), and were able to identify 4 species of hemipterans associated with cowpea production, namely N. viridula, P. guildinii, E. heros, and C. sanctus, the first species being the most abundant. Moreover, the hemipteran diversity on cowpea in our study was similar to that found on other crops, such as soybean in the state of Maranhão, in which 7 species were found (5 were common on cowpea), namely E. heros, T. perditor, C. ubica (= Acrosternum ubicum), P. guildinii, and E. meditabunda (Panizzi 2002).

Fig. 1.

Diversity of hemipterans collected from cowpea crops in Teresina, Piauí, Brazil: (1) Crinocerus sanctus (F.); (2) Hypselonotus fulvus (De Geer); (3) Phthia picta (Drury); (4) Zoreva sp.; (5) Coreidae sp.; (6) Euschistus heros (F.); (7) Euschistus carbonerus (Rolston); (8) Chinavia ubica (Rolston); (9) Dichelops melacanthus (Dallas); (10) Dichelops furcatus (F.); (11) Piezodorus guildinii (Westwood); (12) Edessa meditabunda (F.); (13) Edessa tragulus (Breddin); (14) Edessa loxdalii (Westwood); (15) Thyanta perditor (F.); (16) Mormidea notulifera (Stål); (17) Cyptocephala alvarengai (Rolston); (18) Alcaeorrhynchus grandis (Dallas); (19) Podisus nigrispinus (Dallas).

Fig. 2.

Seasonal abundance (total) and species richness of (A) Pentatomidae and (B) Coreidae collected from cowpea in Teresina, Piauí, Brazil, 2015.

A variety of pentatomids have been reported to feed on different host plants in addition to cowpea in northeastern Brazil. A study by Panizzi (2002) found that E. heros comprised 82.4% of the phytophagous hemipterans collected from soybean in the state of Maranhão. This species is known also as the Neotropical brown stink bug. It is a ubiquitous polyphagous species across Brazil and one of the most abundant hemipterans found on cowpea. Native to the Neotropics, the principal host of E. heros is soybean, but this pest can feed on various other plants, including those of Fabaceae, Solanaceae, Brassicaceae, and Asteraceae (Panizzi & Oliveira 1998). Despite completing fewer generations than other species of soybean-infesting pentatomids, E. heros is the most abundant among them, particularly in warmer regions (Cividanes & Parra 1994; Degrande & Vivan 2010). Our results were similar to those of the above study as mean temperatures at our collection sites were high during the dry and wet seasons when this species was collected.

Fig. 3.

Total abundance of hemipterans, and associated environmental parameters, in collections during (A) rainy season and (B) dry season throughout the phenological cycle of cowpea in Teresina, Piauí, Brazil, 2015.

Fig. 4.

Species of egg parasitoids reared from field-collected Coreidae and Pentatomidae on cowpea crops in Teresina, Piauí, Brazil, (A) Anastatus coreophagus Ashmead; (B) Neorileya flavipes Ashmead; (C) Ooencyrtus anasae (Ashmead); (D) Ooencyrtus submetallicus (Howard); and (E) Trissolcus urichi (Crawford).

Table 2.

Community characteristics of hemipteran species during rainy and dry seasons on cowpea in Teresina, Piauí, Brazil.

Although several species of Chinavia have been reported in northeastern Brazil, only 2 species have been found previously on cowpea in this region, namely C. impicticornis (Stål) and C. ubica (Rolston); however, both species have not yet been reported in the state of Piauí (Schwertner & Grazia 2006, 2007). Chinavia ubica has been collected on cowpea in the state of Pernambuco, on common bean (Phaseolus vulgaris L.) (Fabaceae) in Rio de Janeiro, and on pigeon pea (Cajanus cajan [L.] Huth) (Fabaceae) in the states of Bahia and Rio de Janeiro (Schwertner et al. 2002). Currently, the relationship of C. ubica with its host plants and the damage caused to agronomic crops in northeastern Brazil remains unknown. Also, it should be noted that N. viridula was not collected in our study, even though this species was first reported in northeastern Brazil by Panizzi and Corrêa-Ferreira (1997). However, given the morphological similarities between N. viridula and C. ubica (and the lack of in-depth taxonomic studies) incorrect identification is very likely to have occurred in the past (Schwertner & Grazia 2007).

Despite the scarcity of studies on Pentatomidae in northeastern Brazil, new species of Chinavia and Dichelops have been reported in that region, including C. cearensis Schwertner & Grazia in the state of Ceará, C. tuiucauna Schwertner & Grazia on cocoa plants in the state of Bahia (Theobroma cacao L.), and D. caatinguensis Grazia & Poock-da-Silva collected in the states of Bahia, Pernambuco, and Piauí (Schwertner & Grazia 2006; Poock-da-Silva et al. 2013). Piezodorus guildinii (collected in our study) also is considered to be a major pest of soybeans, beans, peas, and alfalfa, with occasional reports of it feeding on coffee (Rubiaceae), cotton (Malvaceae), guava (Myrtaceae), and sunflower (Asteraceae) in nearby Maceio City, Alagoas State (Firmino et al. 2017).

The polyphagous hemipteran C. sanctus is considered an important pest of cowpea in northern and northeastern Brazil. It was first reported in Brazil in 1984 in the state of Ceará where fairly large populations of this species were collected during the cowpea fruiting stage (Araújo et al. 1984). In our study, this species was observed at the beginning of the fruiting stage but only during the rainy season; no specimens of C. sanctus were found during the dry season.

We collected A. grandis and P. nigrispinus in our sweep net samples. Both species are predators that could be used in integrated pest management programs against phytophagous hemipterans. These 2 species belong to the subfamily Asopinae and have been shown by other workers to have strong potential for use as efficient population regulating agents against lepidopteran and coleopteran pests (Ruberson et al. 1986; Grazia et al. 1999; Lemos et al. 2005).

We observed that parasitoids A. coreophagus, O. anasae, and O. submetallicus were associated exclusively with Coreidae egg masses, whereas T. urichi was associated exclusively with Pentatomidae eggs. Neorileya flavipes was found infesting eggs of both families. These results expand the known range of hemipteran egg parasitoids in northeastern Brazil. This is also the first report of C. sanctus egg parasitism by A. coreophagus and O. submetallicus in Brazil, and the first report of C. sanctus (Coreidae) as a host for N. flavipes, the latter a parasitoid that has been previously reported only in eggs of Pentatomidae by Paz-Neto et al. (2015).

In summary, our study adds to the knowledge of phytophagous hemipteran diversity and associated egg parasitoids on cowpea in northeastern Brazil. Seasonal characterization of the pentatomid and coreid species complex on this agronomic commodity (including interaction of prey with parasitoids) helps to understand population fluctuations during the rainy and dry periods, which would aid in managing hemipteran phytophagous pests in this region of Brazil.