Survey of the Heteroptera (Hemiptera) on pastures from Espírito Santo state, Brazil: new records, range extension, and notes of potential pests

Espírito Santo is a Brazilian state that has a wide variety of habitats, providing a high biological diversity of fauna and flora. However, few reports had been shown about the insect diversity of this region, especially of heteropterans insects that inhabit on pasture ecosystems. In the present study, forty-three species of Heteroptera belonging to thirteen families were collected on pastures on Espírito Santo state, Brazil: Alydidae (1 sp.), Berytidae (3 sp.), Blissidae (1sp.), Coreidae (7 sp.), Miridae (16 sp.), Nabidae (1sp.), Pentatomidae (3 sp.), Pyrrhocoridae (1 sp.), Reduviidae (6 sp.), Rhopalidae (1 sp.), Rhyparochromidae (1 sp.), Thaumastocoridae (1 sp.) and Tingidae (1sp). Among the species; Cebrenis tenebrosa (Brailovsky, 1995) is recorded for the first time in Brazil. The range extension is also included for several heteropterans collected on the Espírito Santo state. The following species: Blissus aff. antillus (Leonard, 1968); Collaria oleosa (Distant, 1883); Oebalus ypsilongriseus (De Geer, 1773), and Trigonotylus tenuis (Reuter, 1893) were observed causing damages on pastures, therefore, in this study, we suggested those species as potential pastures pests. This study aims to increase the knowledge about the heteropterans and to show the presence of some pest species that may cause serious damage to pastures and consequently affect the economy of cattle breeders on the state.

Heteropterans have been studied on both basic and applied aspects worldwide (Panizzi & Grazia 2015) because no other major group of insects successfully utilizes such an enormous array of different habitats (terrestrial, aquatic and semiaquatic) and feeding habits (phytophagous, predatory or hematophagous). It has been inevitable that some of them would become pests of crops. Also, there are some predaceous that would feed on those and could be potential agents of biological control. As a consequence, the interest in heteropteran has been growing especially because many species have become the principal concern in economic and medical fields (SchaeFer & Panizzi 2000).
Among the cultivated plants, Poaceae family is the particular interest of humans. The economic importance of this group of plants is unquestionable, most people on earth rely on grasses, including rice, wheat, and maize, for a major portion of their diet; even to the animals like beef cattle which is raised on diets partly or wholly of grasses (KelloG 2001;euclideS et al. 2010).
Espírito Santo is a Brazilian state that has a wide variety of habitats, providing high biological diversity and resources for various productive activities, both land, and sea (lani et al. 2008). About 4% of its territory is covered by natural pastures (approximately 120,000 ha) and around 43% by planted pastures (approximately 1,220 million ha). However, about 75,000 ha of total pastures of Espírito Santo state are degraded (iBGe 2006).
One of the causes of pasture degradation is attributed to its incorrect management. Pest attack is also a factor that had contributed to this situation (diaS-Filho 2011). Insect attacks on pastures affect directly the capacity of nutrient absorption by the plant, reflecting lower production of meat and milk resulting in economic losses (almeida et al. 2000).
Although heteropterans of several genera are considered a serious pest of pastures, few studies had shown the importance of this group in Brazil. Most studies had focused on the biology and control measures to Scaptocoris carvalhoi,
Espírito Santo state has shown a small number of records and descriptions of Heteroptera species in the pastures and the studies of these species are extremely scarce, elsewhere, among the factors that control pasture productivity may include the understanding of heteropterans complex.
To improve the knowledge of the diversity of species of heteropterans in the pastures of the state of Espírito Santo in Brazil, the authors reported new records of species for the state and country. The distributions for the species on the state and suggestions about potential pasture pests were given.  (Figure 1).

MATERIAL AND METHODS
To generate the map with each sampled site visited, geographic coordinates were obtained with a global positioning system (GPS) using a Garmin GPS (eTREX 10, Garmin, Brazil). All coordinates indicated on the labels of specimens examined are South (latitude) and West (longitude), respectively. The map showing the sampling sites was made with the software ArcMap (version 10.0) (ESRI 2010).
Specimens were collected using beating nets and deposited in plastic bags with pieces of paper and cotton soaked with ethyl acetate, then specimens were mounted in the lab, and examined under a Leica MZ8 stereomicroscope. Whenever required to identify, the genital capsule of males was dissected and cleared with a potassium hydroxide solution for observation. Dissected genitalia was preserved in microvials with glycerin.
All the localities are organized in north-to-south order. All the material examined, including sex and the complete data from the labels, is presented. New records for Espírito Santo state and to the country are indicated with an asterisk (*). When the observations pointed to a particular taxon, but it wasn't identified any character to separate it from others that are very similar, the abbreviation aff., from latin affinis, is used to indicate affinity. In the remarks section, it is shown the Poaceae host plant in which heteropterans specimens were collected. Some pastures in which heteropterans were collected had infested by weeds or crop residuals in the outskirts, the weeds were not identified by specie. However, it was described in the manuscript in general terms.

DISCUSSION
In the present study, forty-three species of Heteroptera belonging to thirteen families were collected on pastures of the Espírito Santo state: Alydidae (one specie), Berytidae (three species), Blissidae (one specie), Coreidae (seven species), Miridae (sixteen species), Nabidae (one specie), Pentatomidae (three species), Pyrrhocoridae (one species), Reduviidae (six species), Rhopalidae (one specie), Rhyparochromidae (one specie.), Thaumastocoridae (one specie), and Tingidae (one specie). Among the species collected; Cebrenis tenebrosa (Brailovsky, 1995)  The vegetational diversity and density in agroecosystems surrounding the pastures influenced the abundance of herbivorous insects as well as their natural enemies (andoW 1983;Schellhorn & SorK 1997). We believe that the association of pastures with weeds and the presence of crop residues improved the records of this study.
Among the forty-three collected species of Heteroptera three of them were observed inducing extensive damage and killing most of the pastures leaves. The species B. aff. antillus; C. oleosa and T. tenuis were collected in many pastures, although only in Tangola grass (Brachiaria mutica x Brachiaria arrecta); Angola grass (B. mutica) and Star grass (Cynodon sp.), respectively were observed causing serious damage. Besides, O. ypsilongriseus was observed feeding of developing grains of bread grass (B. brizantha).
The plant bugs: B. aff. antillus; C. oleosa, T. tenuis, and O. ypsilongriseus are important sapsuckers, those are specialized for feeding especially on Poaceae family plants (Panizzi et al. 2000b;Valério et al. 2015;moraleS et al. 2016;ViVaS & aStudillo 2017). The damages produced by the first three species before mentioned are similar, the youngest leaves attacked can partially or dry out, delaying the growth, reducing yield and nutritional value of the crops and grasses palatability; elsewhere, when the damage of insect is serious its may cause plants death (Valério et al. 2015;ViVaS & aStudillo 2017;Vélez et al. 2020). In the case of O. ypsilongriseus, is considered an important pest of rice in South America, adults and nymphs feeding kernels cause conspicuous areas of discoloration, panicles can be partially or empty and therefore causing losses in the yield and quality of the grain (Panizzi et al. 2000b;ViVaS & aStudillo 2011). The damages of O. ypsilongriseus on pastures seeds need to receive more attention, especially to small cattle breeders that depend on good seeds condition to keep their grasslands.
Therefore, this study helps to increase knowledge about the relationships between heteropterans and pastures. Besides, the timely and accurate identification of heteropterans on pastures could help to recognize among beneficial and harmful insects; establish management strategies to pest insects; prevent the pasture degradation attributed to pest damages, and consequently to avoid losses of dry matter, grass digestibility, which are directly related on the reduction of milk as well as the meat production. Finally, more efforts are still necessary to increase the number of heteropterans species known on the state.