Especies de Hemiptera-Heteroptera asociadas a Opuntia spp. y

The Chihuahuense Desert has an approximate extension of 507 000 km 2 where a vast diversity of organisms is expressed, with a good number of Hemiptera-Heteroptera species present. In this study we determined species of the group in the Chihuahuense Desert, covering six states of the Mexican Republic of this important ecosystem. 10 families of Heteroptera were identified, among them Miridae and Coreidae, in the latter the first report is highlighted of Chelinidea vittiger aequoris Uhler, 1963 for this ecosystem and Cimicidae and Reduviidae, which have medical-veterinary importance.


Introduction
The Chihuahuese desert (DC) is the largest in North America, considered as one of the world's richest dry regions (Morafka, 1977;Sutton, 2000;Hoyt, 2002), has an approximate extension of 507 000 km 2 ranging from center of Mexico (states of Guanajuato, Hidalgo and Queretaro) to the north, in South Texas, New Mexico and a small portion of Arizona.To the west and east is delimited by the Sierras Madre Occidental and Madre Oriental, respectively (Hernandez et al., 2008).Henrickson and Johnston (1986) consider eight primary subdivisions, namely chihuahuense scrub, lechuguilla scrub, izotal forest, Prosopis-Atriplex scrub, alkaline scrub, gypsum scrub, cactus scrub and riparian forest.Rzedowski (1978) named a specific region as a cactus-mesquite thicket, and Miranda and Hernandez (1963) to another as a nopalera.Opuntia spp.species are distributed in different types of vegetation, (Miranda and Hernandez X, 1993); is included in the DC to the arid zone of Tehuacan-Cuicatlan and to the Balsas River Basin (Rzedowskii, 1978).
In Mexico there are more than 100 species of nopales, most of them located in arid zones; these plants have morphological and physiological characteristics adapted to the scarce availability of water, extreme variations in temperature and the conditions of arid and semi-arid zones.In the states of Aguascalientes, Guanajuato, Hidalgo, San Luis Potosi, Zacatecas and part of Jalisco, Michoacan and Queretaro, there is the greatest richness of wild nopal species (35% of total Opuntia spp.) and cultivated varieties (Gallegos-Vazquez et al., 2003).
The national production of nopal vegetables is concentrated in the states of Morelos and Mexico; the most productive states of forage nopal are Coahuila, Aguascalientes and Oaxaca, which has great economic and social importance (SIAP, 2016).Some species of the genus Opuntiaspp.are considered threatened and endangered (Norma NOM-059-ECOL-2001), due to illegal trade, the extraction of their habitats, diseases and insect pests.
The nopales are a relevant resource for Mexico in the ecosystems of arid and semi-arid zones, present in more than 50% of their territory.They are distributed throughout the country, but the highest concentration is in the arid and semi-arid zones of the DC and in the semi-arid zone of Tehuacan-Cuicatlan (Scheinvar et al., 1982), 29 species microendémicas o de distribución restringida, ocurriendo en áreas muy específicas; Las regiones con mayor riqueza de especies son el centro y norte del Altiplano, el noroeste, el Bajío, el Eje Neovolcánico y el Valle de Tehuacán-Cuicatlán.En las regiones tropicales secas y los desiertos del norte hay menor riqueza, pero suelen encontrarse especies endémicas de gran importancia (CONABIO, 2017).
El orden Hemiptera es uno de los más abundantes a nivel mundial.El objetivo del presente trabajo fue conocer la diversidad de Hemípteros del suborden Heteroptera asociados a Opuntia spp.en el desierto chihuahuense.
En cada ruta, cada 100 km, se recolectaban insectos al azar en diferentes especies de nopales silvestres que quedaban aledañas a 200-300 m de uno y otro lado de la carretera, dedicando dos horas en cada sitio.Para recolectar los insectos, se utilizaban cinco formas, manteo, redeo, muestras de suelo, trampas de caída con fruta y directamente con las manos.are microendemic or of restricted distribution, occurring in very specific areas; The regions with the highest species richness are the central and northern Altiplano, the northwest, the Bajio, the Neovolcanic Axis and the Tehuacan-Cuicatlan Valley.In the tropical dry regions and deserts of the north there is less wealth, but endemic species of great importance are often found (CONABIO, 2017).
The Hemiptera order is one of the most abundant in the world.The objective of the present work was to know the diversity of Hemiptera of the suborder Heteroptera associated with Opuntia spp. in the Chihuahuense Desert.

Materials and methods
The insect collections were carried out during the months of July 2016 to May 2017 in different states located in the DC of the Mexican Republic, for which four sampling routes were considered: Route 1. Highway 40, Saltillo-Chihuahua; Route 2. Highway 57, Saltillo-San Luis Potosí; Route 3. Highway 23, Saltillo-Durango, Route 4. Highway 57, Saltillo-Piedras Negras.
In each route, every 100 km, random insects were collected in the different species of wild nopales that were close to 200-300 m on either side of the road, spending at least two hours at each site.To collect the insects, five forms were used, namely, manteo, redeo, soil samples, fall traps with fruit and directly with the hands.
Manteo.Blanket cloth was used to be placed on the ground, under the drip area of nopales or nopal groups and then applied, with a pump 80% Cypermethrin diluted in water, is allowed to pass 30 min to collect clamp or brush was used, very carefully, to the insects fallen on the blanket, which were placed in clear plastic bottles of 100 ml, labeled (collector, date, route, road, kilometer, form of collection) containing 75% ethyl alcohol (v/v).
Redeo.With an entomological network of 30 cm in diameter, at each site, the largest possible number of rounds around nopales was given; the captured insects were placed in flasks labeled with 75% ethyl alcohol.
Direct collection.Nymphs, nymphs, larvae, pupae and insect adults present directly with the hands using tweezers, brushes or mini entomological net were carefully observed, the insects obtained were placed in ethyl alcohol as previously mentioned.
Falling traps.At each site, holes were drilled in the soil underneath nopals to place in the same labeled bottles of 100 mL containing rotten fruits as attractive and whose open mouth remained flush with the soil and remained 1-3 days in accordance with routes (they were placed on the way and picked up on the way back).The captured insects were preserved in 75% ethyl alcohol.
Floor.At each collection site, five soil samples of 1 kg taken 0 to 20 cm deep under nopales were randomly taken; then collected and stirred to take a 1 kg that was put in a bag of labeled paper that was placed in an empty ice maker.
All insects collected by the different methods were transferred to the Insects and Mites Laboratory (LIA) of the Department of Agricultural Parasitology of the Saltillo Headquarters (DPA-S) of the Autonomous University of Agraria Antonio Narro, Campus Buenavista (UAAAN-CB), where considering the routes, sites and forms of sampling were counted and separated first by family, and then to genus and species.

Results and discussion
With the procedures described above, 1 770 insect specimens were collected, of which 750 corresponded to Hemiptera and 719 to Hemiptera-Heteroptera.
En la ruta Chihuahua, se obtuvieron diez familias de Heteroptera; en la de Durango cuatro y en las de Piedras Negras y San Luis Potosí tres.
The number of samples varied between routes, for example, in the one of Chihuahua 14 were realized, in the one of Durango nine and in the one of Piedras Negras and San Luis Potosí, five.
In the route Chihuahua, ten families of Heteroptera were obtained; in the one of Durango four and in those of Piedras Negras and San Luis Potosi three.
The maintenance and the direct collection were the best methods to obtain insects since with them 93% of the total registered was obtained.
The frequency of sampling, type of sampling, time of year, ecological situations, among other aspects, are variables that explain the difference in the number of specimens obtained and the diversity in each of the routes.
In the ten families of insects Hemiptera-Heteroptera associated to Opuntia spp.and Nopalea spp.The 14 genera and 17 species were determined.Ten genera include phytophagous species, two hematophagous species and one predator.At the species level, eleven are phytophagous, three hematophagous and two predators (Table 2).
Coreidae.A taxonomic group with 80 species reported in North America, have developed odorous glands; most are phytophagous, few are predatory (Borror and White, 2005).
Chelinidea vittiger aequoris (Uhler, 1863).It was reported for the first time in Florida (McAtee, 1919;Hamlin, 1924 andTorre-Bueno, 1941).McAtee (1919)  The adult measures from 10 mm to 13.5 mm, pronotum 4 to 5 mm wide, conspicuous back, yellowish orange bands on the head, pronotum yellowish, with yellow veins.The general appearance is very similar to that of the common chants.
Narnia femorata (Stål, 1862).Palomares et al. (2015) reported to N. femorata for the region of Milpa Alta.De Lestang and Miller (2009), mention that these choruses feed mainly on fruits of some opuntia such as O. humifusa, although they also comment that they can feed on cladodes.
For O. ficus-indica, there is no precise information indicating the presence of the insect on this vegetable or the damage it causes (Mann, 1969;Brailovsky and Sánchez, 1983;Lestang and Miller, 2009).Palomares et al. (2015) state that it feeds mainly on tender brambles and feeding points cause a small scar that prevents the growth of the cladodium, taking a heart aspect.
Anasa tristis (De Geer, 1773).Hunter et al. (1912) report it as a pest of the main cacti of the United States of America.Brailovsky (1985) found it on stems of O. streptacantha in Honduras.
Miridae (Hahn, 1831).It is the largest family of the order Hemiptera with about 1 750 species in North America.They have phytophagous and predatory habits; soft body 4-10 mm long marked with red, orange, green or white colors; presence of cuneo and one or two closed cells at the base of the membrane (Borror and White, 2005).
Hesperolabops gelastops (Kirkaldy, 1902).Ruíz et al. (2010) made the first report of H. gelastops in O. ficus-indica in the eastern part of the State of Mexico; the nymphs and adults of the red bug eat sap of the cladodes (Mann, 1969;Badii and Flores, 2001).The feeding of this insect is associated with brown pustules that interfere with the photosynthesis of the plant, which is known as a symptom of the "nopal cactus" (Palomares et al., 2010).
Pentatomidae (Leach, 1815).More than 200 species are known in North America; are recognized by their rounded body to ovoid and antennas of five segments, is divided into the subfamilies, Asopinae, Discocephalinae, Edessinae, Podopinae and Pentatominae.The last four are phytophagous (Borror and White, 2005).
Cimicidae (Latreille, 1802).They are nocturnal insects, flattened, oval, 6 mm in length, hematophagous of birds and mammals; some species are urban pests and attack bats and birds.
Teleonemia scrupulosa (Stål, 1873) Alydidae (Amyot and Serville, 1843).Similar to coreidae, the head is as large as the pronotum and the body is long and narrow.They emit more odors than Pentatomidae (Triplehorn and Johnson, 2005).
Orius laevigatus (Fieber 1860).Laxmi et al. (2015) consider this species as useful in the biological control of insects that affect species of flowers, generally considered to protect different crops, including Opuntia spp.
Lygaeidae (Schilling, 1829).The species present bright colors, orange and black or red and black.They have dorsal abdominal spiracles.They feed on seeds or plants toxic to other organisms.75 species are known in North America (Triplehorn and Johnson, 2005).
Nysius vinitor (Dallas, 1852).The genus Nyzius is cosmopolitan and includes N. californicus Stål and N. raphanus (Howard, 1872) is a major cotton pest.For Mexico other species of this genus are reported as potential pests in various crops such as peanuts, cotton, wheat and malvae (Coronado and Marquez, 1981).Cartron et al. report to Nysius spp. in Opuntia spp.
Reduviidae (Latreille, 1807).Known as killer bugs.It is a group with more than 160 species in North America, they have predatory habits, many species are blackish to cafesuscas or brightly colored, elongated head (Triplehorn and Johnson, 2005).

Conclusions
The diversity of Hemiptera-Heteroptera associated to Opuntia spp. in the Mexican Chihuahuense Desert is diverse and important, since it includes species that are playing different ecological roles in the ecosystem, including phytophagous pests, including nopals, and haematophages of veterinary medical interest.
The Coreidae family is present in abundance with respect to the other families in the Chihuahuense desert.The largest species was C. vittiger aequoris.Abiotic factors as well as number of samples can explain such diversity between sites.

Table 2 . Families, genera and species of Hemiptera- Heteroptera collected in the Mexican Chihuahuan Desert.
Of the total specimens, 353 included four species of Coreidae and 252 to two species of Miridae, respectively, this reference is made because species of Coreidae and Miridae are reported as important pests of Opuntia spp.