Inventory of some families of Hemiptera, Coleoptera (Curculionidae) and Hymenoptera associated with horticultural production of the Alto Valle de Río Negro and Neuquén provinces (Argentina)

. The knowledge of the entomological fauna in productive systems is important for the agroecological management since beneficial insects are a key resource for pest management in horticultural systems. Scientific information on the biodiversity present in a given area is essential as well as the ecological function and/or feeding habits of the insects. In Alto Valle de Río Negro and Neuquén, horticultural production systems can be described as highly dependent on chemical inputs for pest management and fertilization. The aim of this study is to carry out an inventory of the biodiversity of some families of Hemiptera, Coleoptera (Curculionidae) and Hymenoptera present in peri-urban and rural farms located in Neuquén and Río Negro, respectively. Insects were collected through pitfall and sweeping net on tomato and pepper crops and the surrounding non-cultivated areas. Idiosystatus Berg (Auchenorrhyncha) was cited for the first time from Argentina. Species cited for the first time from Neuquén: Hemiptera: Auchenorrhyncha: Acanaloniachloris(Berg), Syncharina punctatissima (Signoret), Amplicephalus dubius Linnavuori, Exitianus obscurinervis (Stål), Agalliana ensigera Oman and Bergallia signata (Stål); Hemiptera: Heteroptera: Harmostes (Harmostes) prolixus Stål and Atrachelus (Atrachelus) cinereus (Fabricius); Coleoptera: Curculionidae: Hypurus bertrandi and Sitona discoideus Gyllenhal and Hymenoptera: Xylocopa (Neoxylocopa) augusti Lepeletier and Pseudagapostemon (Neagapostemon) singularis Jörgensen. Species cited for the first time from Río Negro: Hemiptera: Auchenorrhyncha: AmplicephalusdubiusLinnavuori, AmplicephalusmarginellanusLinnavuori, Circulifertenellus (Baker) and Xerophloeaviridis(Fabricius); Hemiptera: Heteroptera: Tupiocoriscucurbitaceus (Spinola), Atrachelus (Atrachelus) cinereus (Fabricius), Dichelops furcatus (Fabricius) and Harmostes (Harmostes) prolixus Stål; Coleptera: Curculionidae: Naupactus xanthographus (Germar) and Hymenoptera: Diadasia pereyrae (Holmberg) and Dialictus autranellus (Vachal).


INTRODUCTION
Insects make up a large part of the overall diversity in agricultural landscapes and encompass a broad range of functional groups (Kremen et al., 1993). They do not only represent agricultural pest species, insects also serve as biological control agents, provide pollination services, and form an important food resource for many vertebrates in agricultural landscapes (Diekötter et al., 2008).
An increasing number of studies show that the intensification of land uses and homogenization in agricultural landscapes, with the aim of increasing food supply, decreases biodiversity. At the local field scale, increased uses of crop monocultures, greater inputs of fertilizers and pesticides, and decreased within-field heterogeneity may affect species diversity and composition and the provision of ecosystem services to agricultural productivity (Tscharntke et al., 2005).
In the Alto Valle de Río Negro and Neuquén provinces, in the north of the Argentinian Patagonia, the main economic-productive development is linked to fruit production of pears and apples. The second most important activity, in terms of arable land area and impact on the rural economy, is horticultural production (Fernández Lozano, 2012). In this region, both the fruit and vegetable production models can be described as systems highly dependent on chemical inputs for pest management and fertilization (FAO, 2015a(FAO, , 2015b. Besides, the progress of the real estate market and subsequent urbanization on former production areas is affecting the region's biodiversity due to habitat fragmentation. These productive activities take place within a dynamic and heterogeneous landscape. Horticulture farms are surrounded by fruit productive orchards, abandoned orchards, patches and corridors of spontaneous vegetation and poplar "shelterbelts" (e.g., Buck et al., 1999). This landscape heterogeneity provides resources such as nectar and pollen from a diversity of flowering plants, a variety of preys or hosts, and overwintering and nesting habitat for pollinators and predatory insects, which may regulate the incidence of pests and promote the presence of beneficial insects in crops.
Agroecological management has been proposed as an alternative to conventional agricultural management due to its alleged ability to rehabilitate degraded ecosystem services (De Leijster et al., 2019).
The knowledge of the entomological fauna present in productive systems is important for the agroecological approach, since beneficial insects are a key resource for pest management in horticultural systems, allowing a decrease in the use of agrochemicals, and providing other services such as pollination. The maintenance and management of agrobiodiversity is one of the most promising strategies in the search for sustainable agroecosystems. There is a growing consensus that a greater agrobiodiversity in its different dimensions (spatial, temporal, and structural) provides essential ecological services in agroecosystems (Stupino et al., 2014). The growing demand for productive systems with less dependence on chemical inputs promotes the search for management strategies to strengthen ecological processes weakened by a decrease in diversity.
In order to design productive systems with an agroecological approach, it is essential to have scientific information on the biodiversity present in a given area and the ecological function and/or feeding habits of the insects. For example, the order Hymenoptera includes families with a broad heterogeneity of functions: predators (e.g., Vespidae), pollinators (e.g., Apidae), and parasitoids (e.g., Braconidae).
The aim of this study is to carry out an inventory of the biodiversity of some families of Hemiptera, Coleoptera (Curculionidae) and Hymenoptera present in rural and peri-urban horticultural farms, taking into account tomato and pepper crops and the surrounding noncultivated areas (as spontaneous vegetation, abandoned fruit orchards, and poplar shelterbelts).

Study area
Alto Valle de Río Negro and Neuquén is situated in the north of the Argentinian Patagonia, along parallel 39°S and meridians 68°to 66°W (Gili et al., 2004). It develops along the lower basin of Limay and Neuquén rivers and the upper basin of Río Negro river, as seen in Figure 1. Natural and semi-natural habitats, urban centers, peripheries and rural areas are alternated along almost 130 km. The Alto Valle is a long strip about 6 to 20 km wide. The arable land with the highest quality is located near the river terraces of Limay, Negro and Neuquén rivers.
The climate is temperate and semiarid, with an average annual temperature between 13.6°C and 14.5°C and thermal amplitude between 16.1°C and 17.7°C. The rainfall varies between 130 and 170 mm per year, depending on the locality, with a slightly progressive increase from west to east.
It is an area of strong winds higher than 4 m/s on average, with predominant direction southwest-west. The typical vegetation is composed of shrubs of the genera Larrea ("jarillas") (L. divaricata Cav., L. cuneifolia Cav. and exceptionally L. nitida Cav.) and some Prosopis L. such as P. alpataco Phil. ("alpataco"), or Schinus (S. johnstonii F.A. Barkley ("molle"). Permanent and ephemeral grasses grow under these shrubs, although in some areas this vegetation has changed due to the implementation of gravity irrigation system. The usual summer water deficit is mainly supplied by a channel network derived from the Limay, Neuquén and Negro rivers.
In the Alto Valle region, horticultural activities are mostly performed by small and medium farmers. The most important crops are tomatoes, peppers, carrots, pumpkins, lettuce, and other vegetables. The farm activities show strong seasonality depending on the climate (e.g., summer water stress, frost, strong winds, hail) (FAO, 2015a(FAO, , 2015b. Localities studied. The coexistence of peri-urban and rural farms is frequent in the Alto Valle, for that reason we selected one peri-urban farm located on the eastern side of Plottier city (38°57'02.5" S; 68°12'29.5" W), Neuquén province and a rural one located in Campo Grande (38°41'11.5" S; 68°11'25.6" W), Río Negro province. The first one is about 6 hectares in size and belongs to a larger pear orchard (25 hectares in size), abandoned 10 years ago. Currently, this orchard is surrounded by real estate projects with different levels of development (Fig. 1a). The rural farm is about 3 hectares, located in a fruit production area of the Alto Valle. About 20 years ago this area was a pome orchard surrounded by other fruit and vegetable farms. The plot for cultivation is adjacent to the abandoned pear orchard (Fig. 1b).

Collecting insects
For collecting insects in the horticultural systems (peri-urban and rural), we used different sampling techniques, carried out every 30 days, from January to April 2017 (January 6 th , February 3 rd , March 3 rd and

Sampling design
The agricultural landscape was defined as a heterogeneous land area made up of a group of ecosystems, repeated across length and width in similar ways (Forman & Godron, 1986). The landscape represents a mosaic of farms, semi-natural habitats, human infrastructure and, occasionally, natural habitats (Marshall & Moonen, 2002). For this reason, the selected sites included not only tomatoes and pepper crops, but also feral plant communities located on the margins of these crops: abandoned pear orchards, spontaneous vegetation and poplar shelterbelts. Sampling stations were established within each sampling site. The number of stations was based on the site's surface. Each station consisted of the locations where each pitfall trap was placed.

Vegetation sampling
For vegetation sampling we applied quadrat method (Goodall, 1952). At each sampling station a 1 m x 1 m quadrat was randomly placed and all plants within the quadrat were recorded and identified at species level (Kennedy & Addison, 1987), when possible.

Characterization of sites
Peri-urban farm. Tomato and pepper crop. Accompanied by low coverage of herbaceous species (Table I).
Rural farm. Tomato and pepper crop. These crops are accompanied by a low coverage of herbaceous species (Table I).
Abandoned pear orchard. It contains pear, rosehip and wild vine plants within a plantation frame of 6 m x 4 m. Accompanied by an herbaceous stratum where grasses predominate (Table II).
Spontaneous vegetation. It shows the greatest complexity in vegetation structure, with herbaceous, shrub and tree layers (Table II).
Poplar shelterbelt. It is characterized by dominant arboreal species and a medium coverage of herbaceous layer (Table II).
Abandoned pear orchard. It is characterized by a herbaceous layer (Table II).
Spontaneous vegetation. It is characterized by a predominant shrub and herbaceous layers (Table II). Poplar shelterbelt. The arboreal layer of Populus L. "Poplar" is accompanied by a herbaceous shrub layer of medium to low coverage (Table II).

Suborder Auchenorrhyncha
Superfamily Fulgoroidea Family Delphacidae 31 th ), during the period of tomatoes and pepper harvest. The sampling methods were as follows: Sweeping net: Sequential sampling by net blows was carried out to capture the insects that inhabit the aerial part of the vegetation, walking through the field and passing the net over the vegetation. The movement with the net was performed with an angle of approximately 90°. Twenty net strokes were made at each sampling site. The captured insects were placed in transparent jars with 70% ethanol.
Pitfall trap: These traps were used to capture epigeous walking insects. They consisted of 220 ml white plastic containers (diameter: 10 cm; depth, 12 cm), buried and placed at ground level, with 100 ml of a solution of 70% ethanol, 20% water and 10% liquid petroleum jelly. The material obtained by each sampling method was separated for subsequent determination by the authors: Hemiptera  (Table III).
Economic importance. It is a major pest of "maize" in Argentina as vector of MRCV (Remes Lenicov & Paradell, 2012). Table II (Table III).
Economic importance. It is probably another vector of MRCV in central Argentina (Remes Lenicov & Brentassi, 2017 (Table  III and IV).
Phytosanitary importance. Species positive for Xylella fastidiosa Wells et al.

Circulifer tenellus (Baker)
Geographic distribution. Almost cosmopolitan (Nearctic, Palearctic, Oriental and Neotropical regions). In America it is present in Canada, USA, Central American and Caribbean countries, Brazil, Peru, Suriname, Colombia, Venezuela and Argentina (Zanol, 2006). Río Negro is a new province record.
Phytosanitary importance. It is a vector of phytoplasma in Mexico, especially on horticultural plants such as "radish root" and "pepper". It is also vector of Beet curly top virus (BCTV) that produces the Carrot purple leaf (Weintraub & Beanland, 2006;Lee et al., 2006).
Phytosanitary importance. This species transmits the bacteria Spiroplasma kunkelii (Entomoplasmatales: Spiroplasmataceae) under experimental conditions, suggesting that may be a vector of the disease called "Corn Stunt Spiroplasma" in Argentina (Carloni et al., 2011).
Phytosanitary importance. It is a vector of "Virus Sugar Beet Yellow-Wilt" causing the disease "Yellow Wilt" of "sugar beet". This is also a potential vector of fitoplasma 16SrIII X-disease, that causes "Garlic decline" disease (Paradell et al., 2014).  (Tables III and IV).

Superfamily Naboidea
Feeding habits: Predator. Species in the genus are known predators of other Heteroptera, particularly Table III. Order, Family, and species collected in tomato and pepper crops in peri-urban and rural farms. * = new records.
Blissidae, Geocoridae, and Rhyparochromidae (Lattin, 1989). Economic importance. Although the members of Nabidae are generalist predatory species, and some species are frequently present in agroecosystems, the role of nabids in regulation of pest populations of importance to urban agriculture remains largely unknown (Braman, 2000).

Superfamily Reduvioidea
Feeding habits. Predator. Economic importance. No economic damages registered.

Harmostes (Neoharmostes) procerus Berg
Geographic distribution. Argentina: known from all provinces . It has been also recorded for Brazil, Peru, and Uruguay .
Economic importance. No economic damages registered.

Family Lygaeidae
This species has been also recorded for Brazil, Paraguay, and Uruguay (Dellapé & Henry, 2020).
Comments: Although N. simulans is an almost ubiquitous species in Argentina, it is commonly confounded or mixed with populations of other species in the genus, and with species of the closely relative genus Xyonysius.  (Tables III and  IV).  Table IV. Order, Family, and species collected in fruit abandoned orchard, spontaneous vegetation and poplar shelterbelt in peri-urban and rural farms. * = new records. "portulaca". The larvae mine in Portulaca sp. leaves and adults also feed on leaves. Considered a pest in several countries, it is a potential pest in Argentina.
Feeding habits. Phytophagous. Plant associations. It is a primary pest of vegetables, found in many wild and cultivated hosts (more than 80).
Larvae destroy the tender young crown leaves of carrots and turnips. Adults often cause extensive damage by feeding on the leaves of small "tomato" and "potato" plants (Solanaceae), by cutting off the stems of plants at ground level. Females reproduce by parthenogenesis.
Lifecycle. Males are unknown or scarce and the species reproduces by parthenogenesis in most of its range. It is common in pastures, shrubs and crops of the Pampean biogeographic province.
Lifecycle. Adults of N. cervinus feed on foliage and larvae feed on roots. Under severe infestations, these weevils can consume the entire leaf, leaving only the midrib. Plants with severe root damage are more vulnerable to other biotic and abiotic factors (e.g., fungal infections with Phytopthora spp.) and may die during periods of drought. Larval damage can be serious on vegetable crops but relatively minor in citrus. Reproduction occurs without fertilization, a phenomenon known as parthenogenesis, except in small native areas Plant associations. It shows preference for Feeding habits. Phytophagous.
Lifecycle. Adults feed at the bases of leaf margins, leaving characteristic "notching". This feeding behavior injures plants seriously only if adults are very numerous. Larvae gnaw at tap roots, the basal parts of stems and the small lateral roots. When feeding is severe, plants turn yellow, wilt and die. Plants on which only a small amount of the cambium layer is eaten usually survive, but produce little or no crop. In lucerne, the larvae usually chew into the taproot, make a furrow along it and these results in the death of young plants. In "potatoes" damage is more spectacular, as larvae tunnel inside the tubers. The nitrogen fixation rate of Trifolium repens L. is reduced by 92% by N. leucoloma in New Zealand.
Except in some small areas of Argentina, populations of N. leucoloma include only parthenogenetic females.
Geographic distribution. Native to South America (Argentina, southern Brazil, Paraguay and Uruguay (Lanteri & del Río, 2020). Río Negro is a new province record.
Feeding habits. Phytophagous. The adults feed on shoots and leaves, being particularly injurious to young plants. The larvae live in soil during the whole year, eating the plant's roots.

Tribe Otiorhynchini
Otiorhynchus ovatus (L.) Common names. Strawberry Root Weevil Geographic distribution. It is native to Europe and has been introduced in Canada, USA, Australia, New Zealand, Chile and Argentina: Chubut, Neuquén, Río Negro and Santa Cruz. It is considered invasive due to its parthenogenetic reproduction and associations with many plant species.
Geographic distribution. It is native to Europe and
Geographic distribution. It is native to Europe (Palaearctic region) and introduced in several places around the world, North America (broadly distributed), Hawaii, Australia, New Zealand, Japan, Malaysia and Russia. In South America it is present in Chile and Argentina: Chubut, Neuquén and Río Negro provinces. In Argentina it was registered for the first time in 2000 (Lanteri et al., 2002). It is considered invasive due to its parthenogenetic reproduction and associations with many plant species.

Subfamily Xylocopinae
Biological comments. Pollinator. This species nests in solid wood and has a parasocial life behavior (Lucia et al., 2017). Xylocopa augusti is a polilectic species, the presence of 18 pollen types from 11 families of brood cells of several artificial nests was recorded (Lucia et al., 2017). This species presents buzzing behavior to collect pollen and was recorded visiting eggplant crops (Álvarez et al., 2014).

ORDER HYMENOPTERA
nest in the soil and present life habits from solitary to eusocial (Michener, 2007;Dalmazzo et al., 2014).

Family Vespidae
Subfamily Vespinae Vespula germanica (Fabricius) Geographic distribution. Native to the Palaearctic, and introduced in Australia, New Zealand, North America, South America, South Africa, Ascencion Island, Madeira, Canary Islands and Iceland (Beggs et al., 2011). In Argentina it was registered by Willink (1980), and it is distributed from the north of the province of Mendoza to the south of the province of Tierra del Fuego and from the Andes to the Atlantic Ocean (Masciocchi & Corley, 2013;Sola et al., 2015).
Biological comments. Eusocial and with generalist predator behavior, it can negatively affect natural ecosystems and economic activities, including beekeeping, horticulture and tourism (Masciocchi & Corley, 2013).

DISCUSSION
Among the species listed in the present work, 74% are herbivorous, of which 55% are pests, but within this percentage only 35% correspond to horticultural species and the rest to cereals and fruit trees. The remaining 45% of herbivourous species are not pests and can act as alternative prey for predator populations with interest for biological control. Among the nonherbivores (26%) three species are of interest for biological control and five for pollination. It is worth mentioning that only some of the insect families captured in the study are published in the present work. Even so, the species listed herein show the importance of the vegetation areas surrounding the crops. The predatory species were found mainly in the patches of vegetation with greater complexity in their structure since there are herbaceous, shrub and arboreal species (abandoned fruit orchard in the rural area and spontaneous vegetation patch in the peri-urban area), and which also present a greater number of species that represent a source of pollen and / or nectar for insects. Other studies analysing bees, true bugs, and carabids separately in each landscape confirmed that diversity patterns in mosaic agricultural landscapes are strongly determined by the interplay of species' dispersal abilities and landscape structure (Steffan-Dewenter & Tscharntke, 2002;Thomas, 2000). Something similar is observed with species that are pollinators. Floral resource availability is considered a major driving force that directly regulates the abundance and diversity of wild bees' communities (Potts et al., 2003;Roulston & Goodell, 2011).

ACKNOWLEDGMENTS
The authors thank Instituto Nacional de Tecnología Agropecuaria (INTA), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC). This work was supported by INTA and was performed under a specific agreement between INTA-Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata.