Mites on Annonaceae species in northeast Brazil and in the state of Para

The family Annonaceae Juss. comprises over 120 genera and 2000 species with origins in the American, Asian and African tropical regions. Many of these species, such as those of the genera Annona, Rollinia, Duguetia, Uvaria and Asimira, are edible. Some pests have been reported in soursop, sugar apple and atemoya, the main annonas grown in Brazil. However, few mites are mentioned as pests of this plant family. This study aimed to identify mite species associated with the Annonaceae in northeastern Brazil and in the state of Pará. A survey was conducted, collecting samples of Annona muricata L. (soursop), Annona squamosa L. (sugar apples), Annona cherimola × A. squamosa (atemoya) and Annona coriacea Mart. (araticum) leaves. Annona coriacea is a wild Annonaceae widely distributed in northeastern Brazil. For each sample, a total of 100 leaves were collected from five individuals of the same species at each site. The samples were taken to the laboratory, where they were processed and the mites were mounted and identified. The mite species found belonged to the families Ascidae, Bdellidae, Phytoseiidae, Stigmaeidae, Tarsonemidae, Tetranychidae, Tenuipalpidae and Tydeidae. Phytoseiidae, Tetranychidae and Tydeidae had the highest diversity. Five of the reported species were found on all four of the studied cultures: Amblyseius aerialis (Muma), Tetranychus mexicanus (McGregor), Parapronematus acaciae Baker, Pronematus ubiquitus (McGregor) and Agistemus floridanus Gonzáles.


INTRODUCTION
The family Annonaceae Juss.comprises over 120 genera and 2000 species with origins in the American, Asian and African tropical regions.Many of these species are of interest for their edible fruits and are distributed among the genera Annona, Rollinia, Duguetia, Uvaria and Asimira.However, only the first two, especially the Annona, are of economic importance (Mabberley 1997;Nogueira et al. 2005).The genus Annona has approximately 90 species, and its main representatives are Annona reticulata L. (wild sweetsop), Annona muricata L. (soursop), Annona squamosa L. (sugar apples), Annona cherimola Mill.(cherimoya) and the hybrid A. cherimola × A. squamosa (atemoya).Commercial Annonaceae cultivation occurs regionally according to the climatic requirements of each species.The Northeast of Brazil is the main producing region of Annonaceae, especially soursop and sugar apple (Leon 1987;Sobrinho et al. 1998;Cardoso and Sousa 2000;Nogueira et al. 2005).
Several pests, especially insects, are reported in annonas grown in Brazil.However, few pest mites, such as Oligonychus anonae Paschoal (Tetranychidae) and Aculops flechtmanni Keifer (Eriophyidae), have been found to date; both of these species were described in Southeast Brazil (Flechtmann 1985).This study aimed to describe the existing mite fauna in the main cultivated and native Annonaceae species in Northeast Brazil and the state of Pará.

MATERIALS AND METHODS
The study was conducted at the laboratory of Agricultural Acarology in the Agronomy Department of the Federal Rural University of Pernambuco (Uni-  1.
At each sampling site, five plants were chosen.Twenty leaves were sampled from each plant.The samples were taken to the laboratory in plastic bags for further processing.Mites were removed using a stereoscope and a brush, placed in plastic containers containing 70% alcohol and labeled.Subsequently, the mites were mounted in Hoyer's medium and identified by optical microscopy to at least the genus level.

RESULTS
The adult mites identified in this survey belong to eight families, twenty-five genera and thirty-eight species.The families Ascidae, Bdellidae, Phytoseiidade and Stigmaeidae were composed mainly of predator and a few generalist species; the families Tarsonemidae, Tenuipalpidae and Tetranychidae were comprised of phytophagous and one mycophagous species (T.confusus), and Tydeidae included species of polyphagous habits.Among all of the species reported, four (A.aerialis, T. mexicanus, P. acaciae and P. ubiquitus) were found on all the sampled cultures.
A total of 1011 mite specimens were sampled and identified, of which 500 belonged to the Tydeidae family, 162 to Tenuipalpidae, 138 to Tetranychidae, 136 to Phytoseiidae, 47 to Stigmaeidae, 25 to Tarsonemidae, 2 to Bdellidae and 1 to the Ascidae family.

DISCUSSION
The phytoseiid mites had the highest species diversity.Their presence in these microsystems likely indicates environmental balance because most mites are predators that feed on phytophagous mites and insect eggs, while others feed on pollen and are generalists.Most of the mites in this family are studied for use in biological control.Some Phytoseiidae species are widely used in Europe and North America, and new species are still being researched (Moraes 2002).Ten phytoseiid mite species were sampled on A. muricata, six on A. squamosa, seven on A. cherimola × A. squamosa and six on A. coriacea.
The tetranychids A. uncinatus and T. mexicanus and the tenuipalpid B. phoenicis were already reported on annonas species in Brazil (Paschoal 1970b;Flechtmann and Baker 1975;Tuttle et al. 1977;Moraes and Flechtmann 1981).The species B. phoenicis was the most commonly found mite in the sampling sites (12).Among the studied species, this species was not recorded only in A. coriacea.Some Tenuipalpidae mites had already been reported on annonas.Among these mites, the species B. phoenicis was found in Angola (Africa) on A. cherimola, Annona sp. and Rollinia sp.(Meyer 1979). In Brazil, Flechtmann (1976) observed this species on the same host, and Nuvoloni et al. (2011) found this mite on Xilopia aromatica (Lam.).The species T. annonae was described in Mexico on Annona sp.(De Leon, 1957).In this study, T. annonae was found on A. squamosa and A. squamosa × A. cherimolia.In Panamá, Ochoa et al. (1994) observed the species Brevipalpus pseudostriatus Ochoa and Salas on A. cherimola.
A total of six Tydeidae species were reported, five of which were never recorded on annonas in Brazil.Only the species L. formosa was observed on X. aromatica by Nuvoloni et al. (2011).Two of the three species of the Pronematinae (= Iolinidae) subfamily were found on the four studied hosts, while H. anconai was detected on all of the studied plants except atemoya.Among the species belonging to the subfamily Tydeinae, L. formosa occurred on sugar apples, soursop and A. coriacea.Lorryia turrialbensis occurred on all the hosts except for sugar apples, and N. boycei was detected only on atemoya.These mites are not considered plant pests.Some of these mites are mycophagous and may reduce the development of fungi populations, some appear to be alternative prey to Phytoseiidae predator mites, and others are predators.Certain mite species are known for their importance in ecological chains in agroecosystems.Groups of generalist species, such as species of the Tydeidae family, are important in maintaining populations of efficient predator mites and are also alternative food when the preferred prey level is low (Moraes and Flechtmann 2008).Nuvoloni et al. (2011) found Daidalotarsonemus sp. and Tarsonemus sp. on X. aromatica.In the present study, D. folissetae and T. confusus were recorded on A. muricata, D. fossae was found on A. coriacea, and D. tesselatus was found on atemoya.In the Tarsonemidae family, the genus Tarsonemus is composed of micophagous species, and the genus Daidalotarsonemus is composed by species with food habit not well defined.Lindquist (1986) considered that Daidalotarsonenus are probably algophagous or fungivorous, rather than phytophagous, however, Lofego et al. (2005) observed D. tesselatus feed on leaves of Psidium guajava L. In addition to the mentioned species, three new tarsonemid species of were also found on the sampled Annonaceae.Two of these species belong to the genus Daidalotarsonemus and one to Fungitarsonemus, and both of these groups will soon be described.
The family Tetranychidae is composed of strictly phytophagous organisms.Among the reported species, T. mexicanus stood out for occurring on all four of the studied hosts.The species T. neocaledonicus was reported on A. muricata in Australia by Gutierrez and Schicha (1983).Additionally, T. mexicanus and B. phoenicis were found on A. muricata (i.e., soursop) in Água Preta County.These mites are found on leaves in small populations and without causing damage.However, high populations are found on fruits, causing intense darkening, size reduction and induration of healthy fruits.Moraes and Flechtmann (2008) reported these same species in association with damage to the soursop fruit.
The great mite diversity and apparent species equilibrium in Annonaceae detected in this study may be due to the usage of little or no acaricides in these culture systems and to the essentially cultural management of annonas.There are few studies reporting mite species and the damage caused by them on Annonaceae in Brazil.Usually, these mites are identified through surveys of areas involving various plant species of several families.This study demonstrated the great diversity of mites on the plant species belonging to the family Annonaceae in Northeast Brazil and the state of Pará.However, this fauna seems to be in balance, and high populations were not observed, except for T. mexicanus and B. phoenicis on soursop.

TABLE 1 :
State, county, coordinates and host plants.