Mitefauna ( Arachnida : Acari ) associated to grapevine , Vitis vinifera L . ( Vitaceae ) , in the municipalities of Bento Gonçalves and Candiota , Rio Grande do Sul , Brazil

The mitefauna associated to Merlot and Chardonnay grapevine cultivars and associated plants in the municipalities of Bento Goncalves and Candiota, Rio Grande do Sul was investigated. The study was developed between October 2006 and September 2007, where 20 grapevine plants were randomly chosen from each municipality and monthly sampled. Three leaves of each plant were taken. A total of 11,598 mites belonging to 14 families and to 52 species were found. Fifty-nine percent of the total specimens were collected in Candiota, being 93% associated to the Merlot cultivar. Higher species richness was observed on associated plants. Phytoseiidae showed the highest species richness, with ten species, and Eriophyidae showed the highest abundance, with 8,675 specimens. Calepitrimerus vitis (Nalepa, 1905) and Polyphagotarsonemus latus (Banks, 1904) were the most common phytophagous mites, while Neoseiulus californicus (McGregor, 1954) and Pronematus anconai (Baker ,1943) were the most common predators.


Introduction
Grapevine, Vitis vinifera L. (Vitaceae), was introduced in Brazil at 1532 by Martin Afonso de Souza expedition to São Paulo state (Lorenzi et al. 2006).Although it is cultivated today in nearly all regions of the country, the so called 'Serra Gaucha' region of the state of Rio Grande do Sul has currently the greatest vineyards and wineries concentration.More recently, vineyards have been implanted in the well-drained sandy soils of the flatter state region bordering Uruguay and Argentina (Botton et al. 2003;Mello 2008), that seems to be the region with the greatest potential for wine quality.
Grapevine plants are attacked by diseases, insects and mites.Amongst the phytophagous mites, the most important are those belonging to Eriophyidae, Tarsonemidae, Tenuipalpidae and Tetranychidae, since they frequently reach damage level in the vineyards (Reis and Melo 1984;Johann et al. 2009;Schruft 1985;Monteiro 1994;Duso and De Lillo 1996;Botton et al. 2003;Ferreira et al. 2006).
The most important eriophyid mites associated to vineyards are Calepitrimerus vitis (Nalepa, 1905) and Colomerus vitis (Pagenstecher, 1857) (Duso and De Lillo 1996;Jeppson et al. 1975).Three reported strains of Colomerus vitis, being each one characterized by the type of injury produced, are: the bud strain, the erineum strain and leaf-curling strain (Jeppson et al. 1975;Flechtmann 1979;Duso and De Lillo 1996).The symptoms caused by Calepitrimerus vitis was brown scarification and necrosis on the inside of outer bud scales may be found under these mites attack, causing death of the growing point and sometimes of entire buds before sprouting.Injuries caused on shoots are drying, shortened internodes and development of lateral shoots.Injuries on leaves depend already been associated to grapevine, few studies about their predation capacity were carried out.Phytoseiid mites are efficient natural enemies of pest mites of several crops, and its presence is frequently associated with eriophyid mites in Rio Grande do Sul (Ferla pers. obs.), with Euseius alatus DeLeon, 1966, Euseius brazilli (ElBanhawy, 1975), Neoseiulus fallacis (Garman, 1948) and Neoseiulus tunus Denmark and Muma, 1967 already reported on grapevine (Johann et al. 2009;Monteiro 1994).
Despite the economic importance and the damage caused by some phytophagous mites on grapevine in Brazil, little is known about the species associated to this culture.However, because of the increase of the production area and the expansion in the border region of Uruguay and Argentina, it is fundamental to know the mitefauna associated and the damage caused by the most abundant and frequent species.Only then, a management plan to control mites in this culture can be suggested.
The present work aimed to identify the mitefauna associated to Chardonnay e Merlot varieties and associated plants during the harvest of 2006/2007 in the municipalities of Bento Gonçalves and Candiota, in the state of Rio Grande do Sul, Brazil.

Materials and Methods
This study was carried out in vineyards of Chardonnay and Merlot varieties located in the municipalities of Bento Gonçalves (29°13' S, 51°33' W) and Candiota (31°28' S, 53°40' W), between October 2006 and September 2007 (Figure 1).Phytosanitary treatments with acaricides were not conducted during the study in the evaluated areas.The last treatment was applied on the harvest of 2005/2006.
The survey was conducted monthly with twenty plants of grapevine randomly selected from each area.A branch from each plant was sampled, throughout the collection of three leaves from the apical, median and basal regions, respectively, totalizing 60 leaves per area.To evaluate the presence of mites on buds during senescense period, branches from twenty plants were removed and three buds by branch were sampled.Also, leaves from the five most common weeds around the grapevine rows were collected in enough quantity for one hour of sampling effort.
All collected leaves were introduced in paper bags, kept in a cooler box with Gelox® under low temperature (±15°C) and taken to the laboratory, where the material was stored under refrigeration for up to seven days until examination under a stereoscopic microscope for extraction of the mites.Mites found were collected with fine-tipped paintbrush and mounted with Hoyer's medium in microscopic slides (Jeppson et al. 1975).Slides were kept in a kiln during ten days at 50-60 °C to fix, to distend and to brighten up the specimens and to dry the medium.The identification was conducted under phase contrast microscope and with the help of the dichotomics keys (Amrine 1996;Baker et al. 1996;Baker and Tuttle 1994;Chant and McmMurtry 1994, 2003aand b, 2004a and b;2005a, b and c;Halliday, Walter and Lindquist 1998;Krantz 2009;Lindquist 1986;Matioli, Ueckermann and Oliveira 2002;Smiley 1992;Summers and Price 1970).The plants species were identificated by Dra.Elisete Maria de Freitas.
Voucher specimens of each species found were deposited on the mites reference collection of the Museu de Ciências Naturais of Centro Universitário UNIVATES (ZAUMCN), Lajeado, Rio Grande do Sul.

Results and Discussion
A total of 11,598 mites belonging to 14 families were found.Fifty-nine percent of the specimens were collected in Candiota, being 93% associated to Merlot cultivar.
The mites found belonged to 52 species.Phytoseiidae showed the highest species richness, with ten species, followed by Tetranychidae and Stigmaeidae, with six species each, Tydeidae, with five species, and Ascidae, Eriophyidae and Tarsonemidae, with four species each.Eriophyidae showed the highest abundance, with 8,675 specimens, followed by Tarsonemidae, with 1,228 and Tydeidae, with 814.
The mite species and the host plants are presented below, along with the municipality, the cultivar, month and year of collection.Number of specimens is informed in brackets.ASCIDAE Voigts and Oudemans, 1905 Asca sp.
Comments: This species was reported in citrus and yerba mate crops in Taquari Valley, Rio Grande do Sul (Ferla et al. 2005).Species of this genus are common in native vegetation in that state (Ferla and Moraes 2002).Euseius species are polyphagous, but the reproductive potential of many species is highest on pollen (McMurtry and Croft 1997).
Previous records for Brazil: Rio Grande do Sul (Ferla and Moraes 2002).
Comments: The first record of this species in Brazil is by Ferla and Moraes (2002) in native and cultivated plants of Rio Grande do Sul.
Comments: This species belongs to a group of predators that show high oviposition rate when feeding on tetranychid mites (Ferla and Moraes 2003).
Comments: Specialized on tetranychid mites control (McMurtry and Croft 1997).It has been released on apple crop to control P. ulmi and Tetranychus urticae (Koch 1836) in Rio Grande do Sul and Santa Catarina (Monteiro 2002).
Comments: This is the most common predatory mite in plants associated with strawberry in Rio Grande do Sul (Ferla et al. 2007).
Comments: This species of eriophyid mite was reported on viniferous grapevine in Candiota, Rio Grande do Sul (Ferla pers. obs.).
Comments: High populations may attack leaves, producing galls, and buds, causing deformation or even death (Duso and De Lillo 1996).Distribution: It was described from Mexico specimens (Baker 1968).

Criotacus sidae
Comments: This species is an important alternative prey for the predatory mite of Metaseiulus occidentalis (Nesbitt) in California vineyards (Flaherty and Hoy 1971).It feeds primarly on pollen, the predation rate on spider mite eggs is low and it could not reproduce on leaves having only spider mites eggs (Knop and Hoy 1983).PYEMOTIDAE Oudemans, 1937 Pyemotes sp.
Comments: Species associated with yerba mate in Rio Grande do Sul, with higher populations coinciding with eriophyid mites populations peaks (Ferla et al. 2005).Previous records for Brazil: Rio Grande do Sul and Mato Grosso (Ferla and Moraes 2003;Ferla et al. 2007).
Previous records for Brazil: Broad distribution in Brazil (Moraes and Flechtmann 2008).
Comments: It is not a species of economic importance, but it may be considered a potencial cotton pest.It was found in soybean, Glycine max (L.) (1917) Merr., in Rio Grande do Sul (Roggia et al. 2008), where its populations seemed to be increasing in the latest years.
Comments: It is known as yerba mate red mite.It attacks new and ripe leaves, causing brazing and defoliation in severe attacks.During dry and warm periods it attacks in outbreak, usually disappearing after intense rainfall (Flechtmann 1979;Coll and Saini 1992).
Comments: This species is also considered an apple pest, causing leaf brownish, reducing branch growth, size, fruit color and the sugar content, and also causing premature leaf fall.It interferes on the following year's flowering and fructification (Monteiro 2002).It was observed on grapevine in Rio Grande do Sul, where the leaves showed brownish, with reddish branches on adaxial face and premature leaf fall (Ferla and Botton 2008).
Comments: This mite is rather common in Brazil and has been collected from a rather wide range of plants (Flechtmann 1973(Flechtmann , 1987;;Feres et al. 2003;Hernandes and Feres 2006).Populations of this mite may cause sclerotinization of the foliar limb followed by scaling in the area where they are concentrated (Jeppson et al. 1975).
Locality of the specimens examined: Brazil, Rio Grande do Sul, BENTO GONÇALVES: Chardonnay: XII-2006 (1♀), from V. vinifera leaf.Merlot: VII-2007 (1♀), from V. vinifera bud.Mites found in each plant species associated with grapevine sampled are presented in Table 1.The grapevine culture presented great mite richness, higher number of species in Bento Gonçalves (46 species) than in Candiota (21 species).This fact may be related to the recent introduction of the culture in that region or to distinct environmental factors and climate, once Bento Gonçalves is located in the northeast upper slopes, where rainfall and humidity are high, while Candiota is located in west border of the state and has a drier climate and low relative humidity, mainly during the ripening period.

Locality
Calepitrimerus vitis and Cololomerus vitis were the most abundant species, with Cal.vitis being the most common species in the leaves, indicating it is probably the more important phytophagous mite in grapevine in the state.Their monitoring is necessary, because higher populations may cause bud's death decreasing the vegetative growth and leaves brownish with decrease of plant photosynthetic capacity (Duso and De Lillo 1996).The interference on plant photosynthetic capacity also interferes in the quality of the wine produced, since good wines are produced with grapes of good quality (Vencato 2007).
Colomerus vitis was noted only in Merlot cultivar in the two places sampled and populations are much higher in buds.This species may cause deformation in buds and new leaves or still cause the appearance of erinosis of the leaves (Jeppson et al. 1975;Flechtmann 1979;Duso and De Lillo 1996).
Just two tetranychid mite species were observed in Bento Gonçalves.Oligonychus yothersi was found at low density and does not present economic importance to the culture.Panonychus ulmi, present in the two cultivars studied in Bento Gonçalves, was recently reported in the culture in Brazil, with damages described by Ferla and Botton (2008).Commonly associated to Europe grapevine (Jeppson et al. 1975;Schruft 1985;Bolland et al. 1998), it becomes important to the culture in Rio Grande do Sul.Although P. ulmi has not appeared in high density, its finding denotes that this species should be inserted in integrated pest management programs in the state of Rio Grande do Sul.
Four Tarsonemid species were identified and the most abundant were Polyphagotarsonemus latus and Tarsonemus sp.. Polyphagotarsomenus latus was present just in Bento Gonçalves and only on apical leaves.It occurred mainly in January on new leaves after pruning green, suggesting that species did not interfere in vineyard formation (Johann et al. 2009).Nothing is known about the damage caused by this species in that period in grapevine plants.Amongst the predatory mites, the Phytoseiidae presented the higher diversity, mainly in Bento Gonçalves.Neoseiulus californicus, the most common species, was observed in both localities, associated with Cal.vitis.The phytoseiid mite diversity in Serra Gaucha can be related to the presence of tetranychids mites, while low diversity was found in Candiota where this phytophagous group was not found.Tetranychid mites are favorable preys to Phytoseiidae predator mites and the presence of this preys can hold higher number of prey (McMurtry and Croft 1997;Moraes 2002).Neoseiulus californicus has been utilized in program of biologic control of P. ulmi in apple culture with relative success in the states of Rio Grande do Sul and Santa Catarina (Monteiro 2002).In Candiota, the occurence of N. californicus was reported in the same period in which Cal. vitis was found, indicating possible interactions.According to Moraes (2002), there are some species of Eriophyidae that are quite favorable preys to development of phytoseiid mites.Johann et al. (2009), also observed high population of this predator associated with Cal.vitis in Candiota.
The Iolinidae was the most frequent predatory mite and P. anconai was the most abundant species associated with Cal.vitis and P. latus populations, suggesting that it can be an important natural enemy of these species.Species of this family have been reported by Laing and Knop (1982) and Perrin and McMurtry (1996) as predators of eriophyid mites.In Germany, Pronematus staerki Schruft is an important natural enemy of Cal.vitis (Duso and De Lillo 1996).Pronematus anconai was previously reported in the grapevine varieties Alfrocheiro, Cabernet Sauvignon and Pinot Noir in the cities of Bento Gonçalves and Candiota, in Rio Grande do Sul (Johann et al. 2009).
The Tydeidae also showed great species richness (five species) and Tydeus sp. was the most abundant both the localities evaluated.The species was more frequent on leaves during the senescent period, in April and May, and in the bud beginning period.Species of this genus were reported as mites with different feeding habits by several authors.Tydeus caudatus Dugès, T. goetzi Schruft and T. grabouwi Meyer and Ryke were reported as natural enemies of Cal.vitis and Col. vitis in Europe and South Africa (Duso et al. 2004).Representatives of this family were also observed feeding on fungi (Hessein and Perring 1986).The tydeids may have high ecologic importance in agroecossystems to be considered as alternative food to phytoseiid mites (Strickler et al. 1987;McMurtry and Croft 1997;Ferla and Moraes 1998).The consumption of alternative food keeps the predators in the environment where the preferential prey is absent (McMurtry and Croft 1997).
Amongst the Stigmaeidae, Agistemus floridanus was the only species found, with higher population in Bento Gonçalves mainly on Chardonnay cultivar in the same period when Cal. vitis was in high population.According to Ferla and Moraes (2003), Eriophyidae are the most appropriate food to A. floridanus.
The associated plants evaluated in this study containted 39 species of mites, 17 of them as predators.A higher number was collected in Plantago tomentosa, with 163 mites, followed by Solanum sp., with 115 mites.On P. tomentosa 17 species were observed, on Rumex sp., ten species, Senecio sp., nine, on Solanum americanum, eight, on Bidens pilosa and Richardia brasiliensis, seven and on Sida sartaremnensis six species of mites.On strawberry culture, in Rio Grande do Sul, B. pilosa, Rumex sp. and Richardia sp., also presented higher diversity of predator mites (Ferla et al. 2007).
Some associated plants in this study presented low diversity of mites and in 26 vegetal species no mites were found.These results, however, may be under the influence of the sampling frequency whereupon each plant was sampled on different places, so few samples from these plants have been collected.
Uncultured plants occurred naturally and have spontaneous cultivation growth areas.These, in turn, offer many important requirements to natural enemies, such as host and alternative prey, pollen or nectar, as well as microhabitat not available in monocultures free of associated plants (Van Emden 1965).The greater frequency of these plants in agroecosystems can reduce the pest population, since they can hold large predators diversity, and these can naturally migrate from associated plants to cultivated plants (Altieri et al. 2003;Bellini et al. 2005).

Figure 1 .
Figure 1.Location of the municipalities of Candiota and Bento Gonçalves, in the state of Rio Grande do Sul, Brazil.

Table 1 .
Mitefauna of the uncultivated plants associated with grapevine Chardonnay (C) and Merlot (M), in the municipalities of Bento Gonçalves (BG) and Candiota (CA), Rio Grande do Sul, Brazil.