Phytoseiid mites from tropical fruit trees in Bahia State, Brazil (Acari, Phytoseiidae)

Abstract The cultivation of tropical fruit trees has grown considerably in the state of Bahia, northeastern Brazil. Some of these have been severely attacked by phytophagous mites, which are usually controlled by the use of chemical pesticides. However, there is today a growing interest for the adoption of less aggressive measures of pest control, as for example the use of predatory mites. Most of the plant-inhabiting predatory mites belong to the family Phytoseiidae. The objective of this paper is to report the phytoseiid species found in an intensive survey conducted on cultivated tropical fruit trees in fifteen localities of the southern coast of Bahia. Measurements of relevant morphological characters are provided for each species, to complement the understanding of the morphological variation of these species. Twenty-nine species of sixteen genera were identified. A key was elaborated to assist in the separation of these species. Fifteen species are reported for the first time in the state, raising to sixty-six the number of species of this family now known from Bahia. Seventy-two percent of the species collected belong to Amblyseiinae, followed by Typhlodrominae (21%) and Phytoseiinae (7%). The most diverse genus was Amblyseius. Amblyseius operculatus De Leon was the most frequent and abundant species. Studies should be conducted to evaluate the possible role of the most common predators as control agents of the phytophagous mites co-occurring with them.


Introduction
Cultivation of tropical fruit trees has grown considerably in the state of Bahia, northeastern Brazil, in the last years (Santos-Serejo et al. 2009). Several mite species have been reported on those plants, some causing economic losses (Moraes and Flechtmann 2008). These are usually controlled by the use of chemical pesticides.
However, there is today a growing interest on the use of less aggressive and less toxic strategies to control those organisms. Predatory mites of the family Phytoseiidae are considered important biological control agents of pest mites, and some phytoseiids are commercially available for the control of pest mites in several countries (Hoy 2011). There is an interest to implement the use of phytoseiids for the biological control of pest mites in orchards of tropical fruit trees in coastal Bahia, and the determination of the naturally occurring phytoseiids in that area is considered the first step in the implementation of a biological control program.
The objective of this paper is to report the phytoseiid species found in an intensive survey conducted on cultivated tropical fruit trees in the southern coastal region of Bahia, providing a key to help the separation of the species collected.

Materials and methods
Samples were collected from March 2007 to January 2010 in fifteen localities of eight municipalities ( Figure 1, Table 1). These consisted mainly of leaves and, when present, flowers and fruits of 21 species of tropical fruit trees (Table 2).
Phytoseiid mites were mounted in Hoyer's medium, identified and measured under a phase-contrast microscope (Motic® B3 Professional Series). Under each species mentioned in the Results section, information concerning the specimens examined is given in the following order: sampling locality, plant species, month and year of the collection, number and sex of specimens. Measurements are given in micrometers, corresponding to the average for the structures measured followed in parentheses by the respective ranges. Numbers of teeth on the fixed and movable cheliceral digits do not include the respective apical teeth. Setae not referred to in the Results section should be considered absent.
Idiosomal setal notation adopted is that of Lindquist and Evans (1965), as applied to phytoseiids by Rowell et al. (1978) and Chant and Yoshida-Shaul (1989) for the dorsal surface, and by Chant and Yoshida-Shaul (1991) for the ventral surface. Macrosetal notation is that of Muma et al. (1970). The system of classification follows that of Chant and McMurtry (2007). The name adopted for each species is that mentioned in the Phytoseiidae Database (Demite et al. 2014), followed by the names attributed to the species in the original description, in the catalog of Moraes et al. (2004) and in the comprehensive work of Chant and McMurtry (2007).
Voucher specimens were deposited in the mite reference collection of Universidade Estadual de Santa Cruz (UESC), Ilhéus, Bahia.
Remarks. Measurements of the females collected are generally similar to those of the original description, except for the longer Z4, Z5 and s4 in the females measured in the present work [respectively, 77, 86 and 72 in the original description]. Measurements of the females collected differ from those of Moraes et al. (2013) for the shorter j3 and the longer width of dorsal shield, z4, Z4, S2, R1 and calyx of spermatheca [respectively, 33-35, 300-305, 8, 88-92, 98-103, 7-8, 7, 8, 22-23 in the latter]. This is the first record of this genus in Bahia.

Iphiseiodes zuluagai Denmark & Muma
Iphiseiodes zuluagai Denmark & Muma, 1972: 23. Remarks. Measurements of the specimens collected are similar to those of the original description, except for the longer r3 and R1 (2 for the holotype). The calyx of the spermatheca is shorter than reported by Lofego et al. (2009) for specimens from São Paulo state [14 (12-15)]. Measurements of male specimens fit the measurements of the allotype male and those of Lofego et al. (2004). Remarks. Measurements of the females collected are similar to those of the original description, except for longer dorsal shield (263 for the holotype). This is the first description of a male of this species and the first record of this genus in Bahia.

Paraphytoseius orientalis (Narayanan, Kaur & Ghai)
Typhlodromus (Amblyseius) orientalis Narayanam et al., 1960: 394 Remarks. Only measurements of the dorsal shield and of the longer setae were given in the original description. The specimens collected are slightly smaller and concurrently have slightly shorter setae than the holotype. Measurements of the specimens collected are similar to those of the original description of its junior synonym, Paraphytoseius multidentatus Swirski & Shechter, 1961, except for the longer Z5 (76-91 in the latter). They also are similar to the measurements provided by Lofego et al. (2009).

Proprioseiopsis ovatus (Garman)
Amblyseiopsis ovatus Garman, 1958: 78. Remarks. Measurements of the specimens collected fit the redescription of the holotype given by Moraes and McMurtry (1983), except for the shorter S4 and longer width of dorsal shield, J5 and Sge IV [respectively, 23, 252, 4 and 48 in the latter]. The measurements fit the redescription given by Lofego et al. (2009) and Ferla et al. (2011) for Brazilian specimens.

Proprioseiopsis pentagonalis (Moraes & Mesa)
Amblyseius pentagonalis Moraes et al., 1991: 127 Remarks. Measurements of the specimen collected are similar to those of the original description and of Moraes et al. (2013) for specimens from São Paulo state. This is the first record of this species in Bahia.

Typhlodromalus peregrinus (Muma)
Typhlodromus peregrinus Muma, 1955: 270. Typhlodromalus peregrinus: Moraes et al. 2004: 202.  Remarks. Setal measurements were not given in the original description. Measurements of the specimens collected are similar to those of McMurtry (1983), except for the longer Z1 (16-17 in the latter); they also agree with the redescription given by Moraes et al. (2013). Remarks. Measurements of the specimens collected are similar to those of the original description, except for shorter calyx of spermatheca (9 in the holotype). Lofego et al. (2004Lofego et al. ( , 2009) reported a slightly longer Z4 [respectively, 39 (37-41) and 38 (35-45)]. Measurements of the specimens collected are similar to those of Gondim Jr. and Moraes (2001). This is the first record of this species in Bahia.
Remarks. Measurements of the specimens collected are similar to those of the original description.

Phytoseius woodburyi De Leon
Phytoseius ( Remarks. Measurements of the specimens collected are similar to those of the original description, except for the longer St IV (20 in the holotype). Specimens collected in this study have the ventrianal shield longer than reported by Gondim Jr. and Moraes (2001) for specimens from São Paulo state [53 (50-58) in the latter]. This is the first record of this species in Bahia.
Remarks. Measurements of the specimens collected fit the original description. This is the first record of this genus in Bahia.
Remarks. Measurements of the specimens collected fit the redescription of the holotype given by Moraes and McMurtry (1983), except for the longer Z5 (42 in the holotype).

Discussion
Fifty-one phytoseiid species have been reported from Bahia (Bonato et al. 1999;Denmark and Muma 1973;Farias et al. 1981;Fiaboe et al. 2004Fiaboe et al. , 2007Lawson-Balagbo et al. 2008;Lofego et al. 2000Lofego et al. , 2013Moraes et al. 1993Moraes et al. , 1994Moraes et al. , 1997Moraes and Denmark 1999;Moraes and McMurtry 1983;Noronha et al. 1997;Noronha and Moraes 1989;Oliveira et al. 2007;Souza et al. 2010Souza et al. , 2012. In the present study, fifteen species are reported for the first time in that state, raising the number of known species to sixty-six. By far most of the species and of the specimens collected belong to Amblyseiinae (72 and 81%, respectively), followed by the Typhlodrominae (21 and 13%) and the Phytoseiinae (7 and 6%). Similar patterns were summarized by Castro and Moraes (2010) for similar surveys conducted in the Atlantic Forest of southeastern Brazil. There was a general trend for less specific phytoseiid species, i.e., those found on larger number of host plants, to be most abundant. Most of the phytoseiid species was found on a single or few host species. The largest numbers of phytoseiids on C. nucifera, T. cacao and P. guajava suggest that the microhabitat on the leaves of these plants favor these predators, but should not be taken to indicate the preference of these mites for those plants, given that the collecting effort was not the same on all plant species. These higher numbers could be due to the fact that these plants were among the most common in the localities where the study was conducted.
The most diverse genus in the present study was Amblyseius, as also found by Lawson-Balagbo et al. (2008) on coconut palm in the coastal region of Bahia. Amblyseius operculatus was the most abundant species and the species found in the largest number of plants. In total, the total number of specimens of this species was higher than the sum of the second and third most common species, and they were found in every month of the year, except (probably by chance) in February.
A noticeable absence in this study was mites belonging to the genus Euseius Wainstein. Although species of this genus have been reported as diverse and numerous in surveys conducted on different crops in the inland semiarid region of Bahia (Moraes et al. 1993;Moraes and McMurtry 1983), they were not found in the present study nor in previous surveys conducted in the southern coastal region of Bahia (A.R. Oliveira, personal observation) on different plant species.
Total annual rainfall in the semiarid region in the inland of Bahia ranges between 700 and 1,300 mm (Moraes et al. 1993;Moraes and McMurtry 1983), whereas in southern coast it is approximately 1,700 mm, with no pronounced dry season (Almeida and Valle 2010). Daud and Feres (2005) reported significant correlations between the population levels of Euseius citrifolius Denmark & Muma and rainfall (negative) or pollen abundance (positive). Pollen is known to constitute an important part of the diet of Euseius species (McMurtry et al. 2013). Thus, the apparent absence (or scarcity) of Euseius species in the present work could be related to the high rainfall in the southern coastal region and low pollen availability in the tropical fruit trees plantations surveyed. Species of this genus were not rare in a similar survey conducted in the coast of São Paulo state (Castro and Moraes 2010), where rainfall is quite similar to that reported in the southern coastal region of Bahia (Climate-Data.org 2015). This apparent discrepancy could be related to the fact that in that study these species were only found on plants of spontaneous growth, which could be protected at a certain level from the direct effect of rainfall. Those were not sampled in the present study.
The results of this study may contribute to the determination of future research themes, to subsidize future implementation of the use of phytoseiids as biological control agents in the region where the study was conducted. A next step in this trajectory could involve studies under controlled laboratory conditions to evaluate the interactions between the most common predators found and the most common pest species.