Mite fauna of a coffee agroecosystem (Coffea arabicaL.) in the municipality of Monte Alegre do Sul, São Paulo State, Brazil. Part I.

This study aims to assess the mite fauna of coffee plants in the municipality of Monte Alegre do Sul, SP. The sample period was from April 2004 to February 2008. Each month, we sampled 480 leaves and 1,920 fruits from plants of the Coffea arabica L. cv. Mundo Novo. In total 16,062 adult individuals from 30 families representing 81 species of mite (and 1 incertae sedis). Among them, 95% were obtained from leaves, with the Mesostigmata contributing 23 species and 1,805 specimens. The phytoseiid mites were the most abundant, with 1,793 specimens. Seventeen families of Prostigmatid mites were recorded, represented by 48 species and 12,485 individuals. On fruits, the Mesostigmatid mites included three families and eight species. The Prostigmatid mites included nine families and 18 species, totalling 852 individuals. Brevipalpus sp. was the most abundant and frequent species, representing approximately 92% of the Prostigmatid mites. The present work reveals the occurrence of predator mites on coffee plants in the region: Euseius alatus, Amblyseius herbicolus, Iphiseiodes matatlanticae, Armascirus sp.1 and Dactyloscirus sp..


Introduction
The coffee crop is important for Brazilian agribusiness, as the country is the world's greatest producer and exporter, as well as the world's second highest consumer of coffee (MAPA, 2017).
The coffee trees host many species of mites and some of them are pests. Among the most important phytophagous families, the Tenuipalpidae (with the genus Brevipalpus) and Tetranychidae (with the genus Oligonychus) are the main pests of the coffee crops in Brazil (Pallini Filho et al., 1992;Reis and Souza, 1986;Spongoski et al., 2005;Mineiro et al., 2006aMineiro et al., , 2006bReis and Zacarias, 2007). Brevipalpus mites are the main vectors of viral diseases, such as Coffee Ringspot Virus. Other important pest species belong to the genus Oligonychus (O. ilicis and O. yothersi) causing intense defoliation (Reis and Zacarias, 2007).
There are few studies focusing on mites of coffee trees in Brazil and most of them deal only with phytophagous species. Predatory mites, fungivores, and others that are part of the mite fauna in this crop are still poorly studied (Flechtmann, 1967;Pallini Filho et al., 1992;Spongoski et al., 2005;Mineiro et al., 2006aMineiro et al., , 2006b. Thus, it is necessary to assess the diversity of mites in the coffee agroecosystem and especially the species that can act as biological control agents, for improving the integrated pest management programs. This study aims to evaluate mite diversity on the leaves and fruits of coffee trees in Monte Alegre do Sul, eastern region of the State of São Paulo, Brazil.

Materials and Methods
The study was conducted in a plantation, Coffea arabica L. cv. Novo Mundo at São José farm, located in the municipality of Monte Alegre do Sul (Elev. 919 m, 22°40'734" S; 46°38'996" W), one of the main coffee-growing area of the state of São Paulo. This region is characterised by a high concentration of coffee plantations interspersed with forest fragments. The plants were 30 years old and spaced at 3.0 x 2.0 m. One side of the coffee plantation was bordered by the remains of Atlantic Forest in the Serra da Mantiqueira. The climate of Monte Alegre do Sul is classified as CWA (humid subtropical, with rains in summer and droughts in winter) (Setzer, 1966).
Surveys were conducted monthly from April 4, 2004to February 11, 2008. For each date, 480 leaves were randomly sampled from 40 plants (12 leaves per plant), taken from the third or fourth pair of leaves from the distal end of a branch, in the middle third of the plant, according to the methodology described by Pallini Filho et al. (1992) and Mineiro et al. (2006aMineiro et al. ( , 2006b.
From June 2006 to June 2007, six samples of coffee fruits were collected, from 40 plants, with 1,920 fruits obtained per sample. Due to variation in flowering, the collected fruits were those predominant in diameter and colour on the sampled date.
Samples of leaves and fruits were packed in separated paper bags. Each sample was immediately brought to the laboratory inside polystyrene boxes, containing Gelox® to reduce mite activity. For the extraction of mites from leaves and fruits, the collected material was immersed for five minutes in a 70% ethyl alcohol solution. Subsequently, the leaves and fruits were stirred to extract mites, and the solution was filtered through a sieve (with a 0.038 mm mesh). Mites collected on the sieve were stored in 70% alcohol, until analysis. Posteriorly, the mites were mounted on slides in Hoyer´s medium, and for eriophyids a modified Berlese liquid was used for mountings (Walter and Krantz, 2009).
To determine the relation between the mite densities and variables such as temperature and rainfall, a linear regression analyses was performed. The analyses were carried out using BioStat 5.0 program (Ayres et al., 2007). Rarefaction curves were calculated using Past 3.0 program (Hammer et al., 2006).

Results
A total of 16,062 mite specimens belonging to 30 families, 1 Incertae Sedis and 81 species was found. We observed 15,181 individuals and 76 species on leaves and 881 individuals and 29 species on fruits. The Jacknife rarefaction curve estimated 110 species for leaves and fruits ( Figure 1A and 1B).

Leaves
A total of 1,805 Mesostigmata specimens was observed, belonging to 30 families, 1 Incertae Sedis and 23 species. The phytoseiids mites were the most abundant, with 1,793 specimens. The most abundant and frequent species were E. alatus, A. herbicolus, Iphiseiodes matatlanticae Mineiro, Castro and Moraes and I. zuluagai (Table 1).
The Prostigmatid mites contributed to 12,485 individuals, belonging to 17 families and 48 species (approximately 82% of the mites on leaves). The families Tarsonemidae, Tenuipalpidae, and Tetranychidae were the most abundant, together representing 91% of the Prostigmatid mites. Fungitarsonemus sp., Brevipalpus sp. and Oligonychus yothersi (McGregor) were the most abundant and frequent species (Table 2). Brevipalpus mites could not be identified to species level, because a recent review (Beard et al., 2015) shows a complex species within Brevipalpus phoenicis. Thus, we cannot be sure that 3,983 Brevipalpus individuals belong to the same species.
The specimens of four families of Oribatid mites were also observed (35 individuals, 0.2% of mites in leaves). Oripoda sp. was the most abundant species of oribatid (Table 1). Within the Astigmatina mites (856 individuals), three families and five species were recorded. Czenspinskia sp. and Tyrophagus sp. were the most abundant mites. Czenspinskia sp. alone represented 63% of the cohort Astigmatina (Table 1).

Fruits
Twenty-one specimens belonging to three families and eight species of Mesostigmatid were observed (2% of mites on fruits). The phytoseiid mites were the most abundant, with 15 specimens (71% of the Mesostigmatid mites individuals recovered on fruits).
Specimens of Prostigmatid mites (852) belonging to nine families and 18 species were observed (97% of the mites on fruits). Brevipalpus sp. was the most abundant and frequent species, representing approximately 92% of Prostigmatid mites. Exothorhis sp. was the most abundant and frequent species among the predators ( Table 1).
The mites of the suborder Oribatida (Oripoda sp.) and cohort Astigmatina (Tyrophagus sp. and Czenspinskia sp.) were rarely found, with only eight individuals recovered on fruits (Table  1).

Population dynamics on leaf
Euseius alatus was the most abundant and frequent Phytoseiidae species (Table 1), especially in September 2005 and October 2007 (Figure 2). There was a positive correlation between temperature and E. alatus densities, but there was a negative correlation with precipitation (  Figures 2 and 3). There was a negative correlation between temperature and precipitation and A. herbicolus densities ( Table 2, Figures 2 and 3). Iphiseiodes matatlanticae was frequent (66%) and reached 1.2% of phytoseiid mites (Table 1). However, this species was practically absent in September 2006 ( Figure 2). There was a negative correlation between temperature and precipitation and the I. matatlanticae population (    (Figure 2). There was a positive correlation between temperature and precipitation and the densities of Brevipalpus sp. (Table  2, Figures 2, 3). Oligonychus yothersi represented 19% of the total mites and was the most frequent phytophagous species (99%) ( Table 1). There was a positive correlation between temperature and O. yothersi densities and a negative correlation with precipitation (Table 2, Figures 2, 3).

Discussion
The numbers of specimens and species collected in this study are similar to those reported by Mineiro et al. (2006b) in the municipalities of Garça and Jeriquara, SP, in the central-western and northeast regions of the state of São Paulo, respectively. However, the mite populations were much higher than that observed in state of Minas Gerais by Pallini Filho et al. (1992) and Marchetti (2008). The mite diversity on leaves was higher than on fruits, probably due to the higher sampling effort for leaves. Furthermore, the leaves exhibit a greater surface area and they are present for more months than fruits.
Oligonychus yothersi was the most abundant and frequent pest mite, similarly to the studies of  in the municipality of Atibaia (Sao Paulo), and of Marchetti (2008) in Machado, Patrocínio and Viçosa (Minas Gerais). The species most commonly found in coffee in Brazil is O. ilicis (Flechtmann, 1967;Heinrich, 1972;Pallini Filho et al., 1992;Mineiro et al., 2006aMineiro et al., , 2006b. In Costa Rica and Colombia, O. yothersi infestations are reported on coffee trees, with leaf tanning identified as a symptom (Orozco-Hoyos et al., 1990;Ochoa et al., 1991). In a survey conducted by  in Atibaia, there were no symptoms found of tanning on coffee plants. In the present study, no symptoms of leaf tanning were observed.
Phytoseiid mites presented the highest richness of species among predatory mites. Some studies have shown that phytoseiid mites are associated with phytophagous species (Moraes, 1991(Moraes, , 1992Pallini Filho et al., 1992;McMurtry and Croft, 1997;Reis et al., 2000a;Mineiro et al., 2006aMineiro et al., , 2006b, which may contribute to mite pest control. In the present study, E. alatus was the most abundant and frequent phytoseiid mite. This differs from the observations of Mineiro et al. (2006aMineiro et al. ( , 2006b, who found no individual of this species in these surveys.  Euseius species have been reported as effective predators of various species of phytophagous mites in several crops. Euseius alatus is mainly reported in citrus orchards (Moraesand McMurtry, 1983;Sato et al., 1994), coffee (Moraes and McMurtry, 1983;Pallini Filho et al., 1992) in the Southeast, and many other plants in the Brazilian Northeast region (Moraes et al., 1993). Amblyseius herbicolus was also frequent and abundant predatory mite, as also reported by  and Marchetti (2008), in coffee regions of Minas Gerais, and São Paulo (Mineiro et al., 2019). Pallini Filho et al. (1992) concluded that this species is found in association with pest mites, and that result is promising in terms of biological control. The predation and oviposition rates of A. herbicolus increase as the population density of Brevipalpus increases . Iphiseiodes zuluagai was also reported in coffee trees in Minas Gerais (Marchetti, 2008;Silva et al., 2010). Mineiro et al. (2006b) did not record I. zuluagai in the Garça or Jeriquara regions (Sao Paulo state), although this species is frequently encountered in coffee trees in Brazil (Flechtmann, 1967;Pallini Filho et al., 1992;Matos et al., 2004;Spongoski et al., 2005;Silva et al., 2010). The presence of I. zuluagai in coffee crops might be relevant for mite pest management, as predation of Tenuipalpid and Eriophyid pests on citrus has already been proven (Gravena, 1993;Gravena et al., 1994;Sato et al., 1994;Yamamoto and Gravena, 1996). According to Reis et al. (2000b), I. zuluagai can be an important predator of mite species in coffee crops. Stigmaeid mites are biological control agents in various crops, and are considered the second most important predatory mites, after the phytoseiid mites (Matioli et al., 2002). Studies have shown that stigmaeid mites can control mite pests, as Brevipalpus, Phyllocoptruta oleivora (Ashmead), Panonychus citri (McGregor), and O. ilicis (Matioli et al., 1998;Reis et al., 2000a;Sato et al., 2002). The Stigmaeid species reported in this study were similar to those reported by Mineiro et al. (2006a) in coffee trees in the Garça region. In Jeriquara, Mineiro et al. (2006b) reported Zetzellia malvinae Matioli, Ueckermann and Oliveira as one of the most frequent predators. Furthermore, Matioli et al. (2002) observed higher oviposition of A. brasiliensis when supplied with Brevipalpus in comparison with other preys. According to Matioli and Oliveira (2007), A. brasiliensis has a prey preference for Brevipalpus. However, it also feeds on O. ilicis, and thus can be used as a natural biological control agent in coffee plantations in the South and Southeast of the state of São Paulo.
The results of the present study indicated a high richness of mite species on coffee plants in the municipality of Monte Alegre do Sul. However, when compared to other surveys performed in the states of São Paulo and Minas Gerais (Pallini Filho et al., 1992;Spongoski et al., 2005;Mineiro et al., 2006aMineiro et al., , 2006bMarchetti, 2008), some differences in mite diversity were observed. These differences might be due to biotic and abiotic factors such as the surrounding vegetation, soil type, geographical conditions, and precipitation. Further studies are necessary

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Brevipalpus sp. to better understand these interactions and to propose adequate management for an effective biological control.