Redescription of Tenuipalpus heveae Baker (Acari: Tenuipalpidae) and description of a new species from rubber trees in Brazil

Tenuipalpus heveae Baker, 1945 was originally described from only female specimens collected on rubber trees from Belterra, State of Para, Brazil. The original description does not provide enough key information essential for accurate and consistent species identification, and thus, it is difficult to correctly identify this species. In this paper, we redescribe the female, male and immatures of T. heveae, from type and newly collected material, and include additional novel data (e.g. dorsal and ventral ornamentation, leg chaetotaxy and setal measurements) in a standardized form. In addition, we describe Tenuipalpus vieirae n. sp. based on adult females and immatures, collected on Hevea brasiliensis Muell. Arg. and H. guianensis Aubl. (Euphorbiaceae) from Manaus, State of Amazonas, Brazil. We include details of the patterns of ontogenetic setal additions for all stages (except the male of T. vieirae n. sp.) of these two species.


INTRODUCTION
Some researchers have recorded a high abundance of Tenuipalpus heveae Baker (Acari, Tenuipalpidae) on rubber tree plantations, Hevea brasiliensis (Euphorbiaceae), in different regions across Brazil (Hernandes & Feres 2006;Daud & Feres 2007;Castro et al. 2013). According to Pontier et al. (2000), high infestations of T. heveae may cause leaf rusting followed by plant defoliation. Currently, this mite species is considered to be a pest for this crop in several states of Brazil (Castro et al. 2013).
The original description of Tenuipalpus heveae was based only on adult female specimens collected on rubber trees in Belterra, State of Pará, Brazil (Baker 1945;Baker & Pritchard 1953). Recently, male and immatures were described by Pontier & Flechtmann (1999;2000), respectively. However, these descriptions does not provide enough key information essential for accurate and consis-tent species identification (e.g. dorsal and ventral ornamentation, leg chaetotaxy and setal measurements), and thus, it may be difficult to correctly identify the species. The objective of this paper is to redescribe the female, male and immatures of T. heveae in a standardized form, and describe a new species collected on rubber tree from Manaus, State of Amazonas, Brazil.

MATERIALS AND METHODS
Measurements of the holotype are given in micrometers (µm), with the range of measurements for the paratypes shown in parentheses. Photographs taken using differential interference contrast (DIC) microscopy are included. The terminology used follows that of Lindquist (1985) and Mesa et al. (2009). Leg chaetotaxy is adapted from Lindquist (1985), Xu & Fan (2010) and Seeman & Beard (2011). Tarsal setae are presented as the total number followed by the number of solenidia in parentheses.
Specimens of T. heveae were collected on Hevea brasiliensis Muell. Arg. (Euphorbiaceae) from São José do Rio Preto, State of São Paulo, Brazil. These specimens were maintained in 70% ethanol and later used for low-temperature scanning electron microscopy (LT-SEM) studies. Mites for LT-SEM studies use the methodology previously described by Castro et al. (2015). Non-type material of T. heveae was collected from rubber tree plantations of different regions of Brazil.
Type specimens and voucher of non-type material are deposited in the Collection of Acari, Departamento de Zoologia e Botânica, UNESP, São José do Rio Preto, State of São Paulo, Brazil (DZSJRP, http://www.splink.cria.org.br) and in the National Insect and Mite Collection, National Museum of Natural History, Smithsonian Institution, located in the Systematic Entomology Laboratory (SEL), USDA, Beltsville, Maryland, USA (NMNH).
Color ( Figure 2a) -The body is reddish with the margin of prodorsum and opisthosoma darker red. The legs and dorsal setae are orange. Due to its color, this species is known in Brazil as the rubber tree red false spider mite or "falso-ácaro-vermelhoda-seringueira".
Hosts and distribution -This species has been collected on rubber trees from several Brazilian states, and occurs mainly on the lower surface of the leaflets.
Remarks -The non-type specimens examined in this study have similar body and setal measurements to those of the type specimens (Table 2). In addition, the pattern of dorsal ornamentation and the leg chaetotaxy of those specimens match those of the type specimens.
Leg I
Color -The body is dark red with some black spots. The legs are red. Leg and dorsal setae are orange.
Hosts and distribution -On two species of rubber tree, Hevea brasiliensis and H. guianensis, from the State of Amazonas, Brazil. This species occurs mainly on the upper surface of the leaflets.
Etymology -This species is named in honor to Dr. Marineide Rosa Vieira, of the Universidade Estadual Paulista-UNESP, campus de Ilha Solteira, SP, Brazil, a Brazilian Acarologist who has been contributing to the study of rubber tree mites.
Remarks -This new species belongs to the Tenuipalpus sensu lato group (Castro et al. 2016b). It resembles Tenuipalpus heveae Baker, 1945 in that it shares a similar pattern of ventral striations and shapes of the leg setae, but T. vieirae n. sp. has different features of the dorsum and leg chaetotaxy to T. heveae. In T. vieirae n. sp., the dorsum is smooth, versus heavily ornamented in T. heveae; setae sc1, c3, e3 are smaller on T. vieirae n. sp. than those setae on T. heveae; the anterior median projections on the prodorsum are longer on T. vieirae n. sp. than on T. heveae. The chaetotaxy differences are: trochanter 1-1-2-1 in T. vieirae n. sp. and 1-1-1-1 in T. heveae (l' absent on trochanter III); tibia 5-5-3-2 in T. vieirae n. sp. and 5-5-2-2 in T. heveae (d absent on tibiae III). In addition, setae bv" on femora II and setae d on femora III are shorter and much broader on T. vieirae than those setae on T. heveae.

ONTOGENY
Tenuipalpus heveae and T. vieirae have setae v' on trochanters I, II and III added in the deutonymph and on trochanter IV in the adults. This is the standard pattern for other Tenuipalpus (Welbourn et al. 2017) and also for Tetranychidae (Lindquist 1985). Setae l' on trochanters III appears in the protonymph of T. vieirae and is not present in T. heveae. The expression of setae l' on the protonymph is common in the Tenuipalpidae (de Castro et al. 2015;Khanjani et al. 2013). Tenuipalpus spinosaurus Castro, Feres & Ochoa (2016) and the new species described by Welbourn et al. (2017) have the expression of l' unusually delayed one stage to appear in the deutonymph, with v'. The absence of setae l' on trochanter III is not common in Tenuipalpus, but it does occur in related taxa, such as Gahniacarus and Prolixus (Beard & Ochoa 2011;Xu & Zhang 2014). While comparing species of Tenuipalpus, an examination of the type specimens of T. tapiae (De Castro & Feres 2013) revealed some errors in the setal count for legs in the protonymph and deutonymph. The correct setal count for trochanters I-IV in the deutonymph is 1-1-2-0, and not 1-2-2-0, and the addition of setae is similar to that found here.
Setae l' are added to femora I and II in the deutonymph of T. heveae and T. vieirae, and this pattern of expression on the femora appears to be common in the taxon Tenuipalpus (Khanjani et al. 2013;de Castro et al. 2015b;Castro et al. 2016a), and in the family Tetranychidae (Lindquist 1985). Seta l' is also added to femora I-II in the deutonymph of Acaricis, Prolixus and Lisaepalpus (Welbourn et al. 2017). Seta l' is also added to femora I-II in the deutonymph of T. tapiae, and the protonymph have three setae (d, v', bv"), not four as in De Castro & Feres (2013). Tenuipalpids usually have similar setal count on femora I-IV in both the female and male adults, with the exception of setae l" being added only in the male of P. corruginus (Xu & Zhang 2014).
Tenuipalpus heveae and T. vieirae have setae d added on genua I-II in the deutonymph and setae on genua III-IV are suppressed (1-1-0-0). Tenuipalpus toropi and T. spinosaurus have l' present on genua I-II in the larva and protonymph, and add setae l" and d to genua I-II in the deutonymph, and seta d to genu III in the deutonymph, while genu IV remains nude (3-3-1-0). Setae d are also added on genua I-II in the deutonymph of T. tapiae, not in the protonymph as listed in De Castro & Feres (2013). Prolixus corruginus have setae l' added on genu II only in the adult male (Xu & Zhang 2014), while most of tenuipalpids have similar setal count on genua I-IV in both females and males.
The number of tibial setae is 5-5-2-2 in T. heveae and 5-5-3-2 in T. vieirae, with setae d on tibiae III-IV being suppressed in the former, and suppressed only on tibia IV in the latter. The most common pattern of tibial setae for Tenuipalpus is 5-5-3-3 (Baker & Tuttle 1987;Meyer 1979), while this pattern varies across other tenuipalpids taxa, e.g. Dolichotetranychus have l" absent on tibiae I-II (4-4-3-3). These tibial setal counts represent the larval complement and no post-larval additions are made to tibiae I-IV in the Tenuipalpidae (Lindquist 1985).
Tenuipalpus heveae and T. vieirae have a pair of tectal setae added to tarsi I-II in the deutonymph, and only setae tc" are added to tarsi III in the deutonymph and to tarsi IV in the adult. Setae tc' are not expressed at all on tarsi III-IV of these two species. The addition of tectal setae normally occurs in the protonymph on tarsi I-III, and in the deutonymph on tarsi IV (Lindquist 1985). Here the additions are delayed one stage. This pattern is shared by other species of Tenuipalpus, for example T. toropi and T. tapiae (setal count to tarsi I-IV in the protonymph of T. tapiae is 7(1)-7(1)-3-3, and not 8(1)-8(1)-4-3 as listed in De Castro & Feres (2013)). This pattern is similar to that found on Tenuipalpus sarcophilus Welbourn & Beard (2017) and on T. spinosaurus, except that these two species add setae tc" to tarsi III in the deutonymph and to tarsi IV in the adult (9(1)-9(1)-5-5). The pattern of additions to the leg chaetotaxy during ontogeny in T. heveae and T. vieirae is listed in Table 1.
The posterior ventral setal changes are as follows: ag is added in the protonymph, 4a and g1 appear in the deutonymph and g2 is added in the adult. This pattern of ontogenetic additions is the same as the general pattern observed for Tetranychidae by Lindquist (1985). All setae of the gnathosoma are present in the larva, except setae m which are added in the protonymph.

DISCUSSION
Systematics of mites has greatly improved due to the critical study of all stages of development using differential interference contrast microscopy (DIC) and particularly the Low-Temperature SEM (LT-SEM). The use of the LT-SEM has made it possible to observe mites at extremely high magnification (up to 20,000x) and resolution. This has greatly enhanced the ability to identify new characteristics, in addition to recognizing key identifying traits to distinguish mites and thus, develop and produce vitally important taxonomic studies of mites. Although T. heveae is considered a pest of rubber tree plantations in Brazil (Pontier & Flechtmann 2000;Ferla & Moraes 2008), prior to this study, key details of the female, male and immatures (e.g. leg chaetotaxy and setal measurements) have not been described adequately enough to allow its correct identification. The new species described here, T. vieirae n. sp., occurs on the same host plant as T. heveae and this increases the necessity and importance of a description detailed enough to allow the consistent and reliable differentiation between these two species. It is important to note that T. heveae occurs mainly on lower surface of the leaflets, while individuals of T. vieirae n. sp. are found on the upper surface of the leaflets (F.M. Nuvoloni, pers. comm.). This difference may be useful in the identification of these two species. In addition, T. heveae is recorded in rubber plantations from several states of Brazil (Daud & Feres 2007;Hernandes & Feres 2006), while T. vieirae n. sp. is described here from only specimens collected in the Amazonas state. To date, there is no record of this species in other localities. We believe that this new species may not be adapted to climatic conditions (e.g. temperature and air humidity) present in the other regions of Brazil where the rubber tree is more commonly cultivated.