We report here on the diversity and composition of Coreidae and Pentatomidae species, as well as their egg parasitoids collected on cowpea (Vigna unguiculata [L.] Walp) (Fabaceae) plants from a field in Teresina, central-northern Piauí State, Brazil. Weekly sweep net sampling was performed during the phenological cycle of this crop in the rainy and dry seasons. In the pentatomid collections, 14 species were identified from 3 subfamilies (Asopinae, Edessinae, and Pentatominae). Five species of Coreidae also were collected from the subfamily Coreinae. We found that Euschistus heros (F.), Crinocerus sanctus (F.), Chinavia ubica (Rolston), and Piezodorus guildinii (Westwood) (all Hemiptera: Pentatomidae) were the most abundant hemipteran species associated with cowpea. Generally, species richness and diversity of individuals from this order were higher in the rainy season than in the dry season. The parasitoid species identified from field-collected hemipteran egg masses were: Anastatus coreophagus Ashmead (Hymenoptera: Eupelmidae), Neorileya flavipes Ashmead (Hymenoptera: Eurytomidae), Ooencyrtus anasae (Ashmead) (Hymenoptera: Encyrtidae), O. submetallicus (Howard) (Hymenoptera: Encyrtidae), and Trissolcus urichi (Crawford) (Hymenoptera: Platygastridae). We found that about 52% of hemipteran egg masses collected from the cowpea field were naturally parasitized by the above parasitoids, whereas nearly 10% of C. sanctus and C. ubica sentinel egg masses were parasitized.
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
This study was conducted in northeastern Brazil near the city of Teresina located in the north-central portion of the state of Piauí, situated on the right bank of the Parnaíba River, in the middle course of its catchment basin. According to the Köppen classification system, climate in the area is tropical with seasonal rainfall concentrated in the summer-autumn months; vegetation in this area is primarily subdeciduous forest characterized by cerrado and caatinga-like habitats. Caatinga means “white forest” in the native Tupi language, and is typified by small trees, thorny brush, arid grasses, and thorny, often leafless, scrub vegetation in the dry season. This ecosystem commonly occurs in areas of minimal rainfall in northeastern Brazil. The cerrado ecosystem is a tropical savanna composed of vast grassland with scattered trees.
The cowpea field used in this study was located on an experimental field owned by Embrapa Meio-Norte in Teresina (5.039266°S, 42.789566°W). Two fields were planted with the BRS Maratoã variety of cowpea, totaling 500 m2 with 0.70 m of spacing between rows. For the crop grown during the rainy season, plant emergence started on 26 Mar 2015, whereas a second crop (grown during the dry season) started emergence on 25 Aug 2015. During the experiments, cowpea crops in each field were cultivated similarly using accepted crop production practices. Irrigation was performed during the dry season by sprinkling every 2 d. The only insecticide used on plants for control of defoliating caterpillars was a commercial Bacillus thuringiensis product. Weeds were managed by mechanical removal. Weekly climatic data, i.e., rainfall, relative humidity, and temperature, were obtained from the meteorological station at Embrapa Meio-Norte in Teresina, in the same vicinity where the experiment was conducted.
POPULATION SURVEY OF COREIDAE AND PENTATOMIDAE SPECIES
Weekly sampling was performed during the cowpea phenological cycle during the rainy (Apr–Jun 2015) and dry seasons (Sep–Nov 2015). Hemipterans were collected using a sweep net, with 10 sweeps at each of the 36 sample locations arranged along linear transects. Samples were stored in plastic containers filled with 70% ethanol, tagged, and placed in a freezer. Specimens were separated later into morphotypes, counted, and photographed (Choate 2000). Identification to the species level used the taxonomic keys of Rolston and McDonald (1980, 1984), Thomas (1992), Packauskas and Schaefer (1998), and Grazia and Schwertner (2008), including assistance from Pentatomoidea taxonomists Jocelia Grazia (Federal University of Paraná) and José Antônio Marin Fernandes (Federal University of Pará).
HEMIPTERAN EGG PARASITISM
Naturally occurring parasitism by Hymenoptera was assessed by collecting hemipteran eggs in the field and setting out sentinel egg masses. Egg masses were hand collected from the cowpea field, identified, stored in containers, and maintained in a growth chamber (PRLABOR, model 4102, Cascavel, Paraná State, Brazil) at 25 ± 2 °C, 70 ± 10% RH, and 12:12 h (L:D) photoperiod until parasitoids emerged. As an additional measure of parasitoid activity in the field, sentinel egg masses (previously deposited on paper cards in Petri dishes) also were affixed to cowpea plants. Sentinels were produced from adult C. sanctus and Chinavia ubica Rolston (Hemiptera: Pentatomidae) previously reared in the laboratory from field-collected eggs. After 72 h, cards were retrieved and placed in growth chambers until parasitoids emerged. Parasitoids from all egg masses were identified to species according to Johnson (1984a, 1984b, 1985, 1987a, 1987b) and Noyes (1985, 2010). Voucher specimens were deposited in the Entomology Collection at Embrapa Meio-Norte, Teresina, Piauí, Brazil.
Faunistic analysis of collection data for abundance, diversity, species richness, and uniformity or evenness was performed using the ANAFAU software (Moraes et al. 2003). Climatic data were obtained from the weather station at Embrapa Meio-Norte in Teresina, and were used to analyze the relationship among hemipteran abundance, humidity, temperature, and precipitation, applying the Pearson correlation coefficient (r) (Ludwig & Reynolds 1988).
DIVERSITY OF PENTATOMIDAE AND COREIDAE
Pentatomids sampled from cowpea were represented by 3 subfamilies, from which 14 species were identified (Table 1, Fig. 1). The species from subfamily Pentatominae were: C. ubica, Euschistus heros (F.), E. carbonerus Rolston, P. guildinii, Thyanta perditor (F.), Cyptocephala alvarengai Rolston, Mormidea notulifera (Stål), Dichelops melacanthus (Dallas), and D. furcatus (F.). The specimens from the subfamily Edessinae were: Edessa meditabunda (F.), E. loxdalii Westwood, and E. tragulus Breddin, and the subfamily Asopinae was represented by Alcaeorrhynchus grandis (Dallas) and Podisus nigrispinus (Dallas). Individuals of Coreidae collected from cowpea, represented by the subfamily Coreinae, consisted of C. sanctus, Hypselonotus fulvus (De Geer), Phthia picta (Drury), Zoreva sp., and an unknown Coreidae sp. 1 (Table 1, Fig. 1).
The hemipteran species collected in this study were classified into 2 trophic guilds (phytophagous and predator) based on diet-related functional groups. A greater number of phytophagous species was collected (17 species) compared with only 2 species of predator hemipterans. The richness of species and abundance of hemipteran populations varied across the phenological stages of cowpea. Pentatomidae species increased in abundance and richness from the start of the vegetative growing period during the rainy and dry seasons (Fig. 2a). Increased species richness and abundance of Coreidae populations occurred during the reproductive stage of the crops (Fig. 2b).
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).
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).
PARASITOID SPECIES ASSOCIATED WITH HEMIPTERANS
A total of 130 hemipteran egg masses were monitored for parasite emergence; of those 23 were collected from the field and the rest represented by sentinels. Natural parasitism occurred in 51.9% of egg masses collected from the field and 9.7% of sentinels. The parasitoid species identified from naturally parasitized field-collected egg masses were Neorileya flavipes Ashmead (Hymenoptera: Eurytomidae) (obtained from C. ubica and Chinavia sp. eggs), as well as 2 unidentified species from pentatomid eggs. Trissolcus urichi (Crawford) from eggs of E. heros and C. ubica also were recovered. Sentinel eggs of C. ubica were parasitized only by N. flavipes, and those of C. sanctus were parasitized by Anastatus coreophagus Ashmead, Ooencyrtus anasae (Ashmead), O. submetallicus (Howard), and N. flavipes (Fig. 4).
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).
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.
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.
The authors express heartfelt gratitude to the National Council for Scientific and Technological Development (CNPq) for financial support (No. 456197/2014-1). We also thank José Antônio Marin Fernandes (Federal University of Pará). We are also grateful for valuable comments on the manuscript from anonymous reviewers and the editor of the journal.
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