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

Castro, Elizeu B.1; Ramos, Felipe A.M.2; Feres, Reinaldo J.F.3; Ochoa, Ronald4 and Bauchan, Gary R.5

1✉ Programa de Pós Graduação em Biologia Animal, Universidade Estadual Paulista-UNESP, campus de São José do Rio Preto, São Paulo, Brazil.
2Universidade Estadual Paulista-UNESP, campus de S. J. do Rio Preto, São Paulo, Brazil.
3Depto. de Zoologia e Botânica, UNESP, Rua Cristovão Colombo, 2265, Jardim Nazareth, S. J. do Rio Preto, São Paulo, Brazil, 15054-000, CNPq-Brazil researcher.
4Systematic Entomology Laboratory (SEL), Agricultural Research Service (ARS), United States Department of Agriculture (USDA), Beltsville Agricultural Research Centre (BARC), Beltsville, Maryland, 20705, USA.
5Electron and Confocal Microscopy Unit (ECMU), ARS-USDA, BARC, Beltsville, Maryland, 20705, USA.

2017 - Volume: 57 Issue: 2 pages: 421-458

DOI: 10.1051/acarologia/20174166
ZooBank LSID: 0763BBAE-D697-4E4A-89D3-C49CDAEC6265

Keywords

Hevea sensu lato group Tenuipalpus vieirae red false spider mite pest mite ontogeny taxonomy systematics

Abstract

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 consistent 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).

Family Tenuipalpidae Berlese, 1913
Genus Tenuipalpus Donnadieu, 1876

Type species — Tenuipalpus palmatus Donnadieu, 1876 (=T. caudatus (Dugès, 1834))

Diagnosis — (Following Castro et al. 2016a). Female: Body shape with prodorsum wider than opisthosoma or elongate-ovate; prodorsum with three pairs of setae (v2, sc1, sc2; except v2 absent in T. elegans (Collyer)); dorsal opisthosoma with eight to ten pairs of setae (c3, d3, e3, f3, h1, h2 present; c2, d2, e2 absent; c1, d1, e1, f2 present or absent (d1, e1 rarely absent); setae h2 elongate, flagellate. Palp one to three segmented. Venter with one to two pairs of setae 3a (3a always present; 3a2 present or absent) and one to four pairs of setae 4a (4a always present; 4a2, 4a3, 4a4 present or absent); ventral and genital plates not developed, membranous genital flap present; commonly two pairs of pseudanal setae ps2-3 present (three pairs, ps1-ps3, rarely present). Male: Opisthosoma distinctly narrower than that of female; legs and dorsal setae usually similar to those of female; pseudanal setae ps3 modified as accessory genital stylet.

Results
Tenuipalpus heveae Baker

(Figures 1-17)

Tenuipalpus heveae Baker, 1945: 36; Baker & Pritchard, 1953: 319; Pontier & Flechtmann, 1999: 293; Pontier & Flechtmann, 2000: 77.

Diagnosis — Female: Dorsum completely ornamented; prodorsum with transverse to oblique striae, and pair of converging oblique ridges from sc1 to sejugal furrow (weakly evident under DIC, strongly evident under SEM); triangular to semicircular plate weakly evident encompassing c3-d3. Anterior margin of prodorsum with pair median triangular projections, forming a notch. Dorsum with setae v2, c1, d1, d3, e1 minute; setae sc1, sc2, c3, e3, f2, f3, h1 ovate to lanceolate, barbed; h2 elongate, flagelliform; f2 present. Palps three segmented. Ventral integument with regions of smooth cuticle and with regions of fine longitudinal striae; striae oblique and converging to become longitudinal striae between 3a setae; ventral prodorsum with lateral margin longitudinally striate; striae surrounding coxae III and IV oblique; large region of smooth cuticle laterad setae 4a-ag; broken transverse striae between setae ag and g1-g2. Coxal setae 1b and 2b filiform and smooth, other coxal setae sparsely plumose. Tarsi I-IV 9(1)-9(1)-4-4 (setae tc' absent on tarsus III-IV); trochanters I-IV 1-1-1-1 (seta l' absent on trochanter III); setae d absent on tibia III and IV. Male and immatures: most of dorsal setae similar to those of female.

Type material examined — Holotype: female collected on a rubber tree, Hevea brasiliensis Muell. Arg. (Euphorbiaceae), Belterra, State of Pará, Brazil, 9 Aug. 1941, coll. J.A. Zilles, deposited in National Insect and Mite Collection, National Museum of Natural History, Smithsonian Institution, located at the SEL-USDA, Beltsville, Maryland, USA (USNM no. 1481a). Paratypes: 2 females with the same data as the holotype (USNM no. 1481b–1481c); 1 female with the same data as the holotype, deposited in Collection of Acari, Departamento de Zoologia e Botânica, UNESP, located at the São José do Rio Preto, State of São Paulo, Brazil (DZSJRP no. 10145 (donation of slide USNM no. 1481d)).

Non-type material examined — 5 females collected on H. brasiliensis from Igrapiúna, Bahia, Brazil, 2009; coll. E.B. Castro (DZSJRP n. 10146–10148); 2 females collected on H. brasiliensis from Manaus, Amazonas, Brazil, 20 Oct. 2000, coll. T.J. Izzo; 2 females collected on H. guianensis Aubl. (Euphorbiaceae) from Manaus, Amazonas, Brazil, Aug. 2012, coll. F.M. Nuvoloni (DZSJRP n. 10149–10151); 3 females collected on H. brasiliensis from Taquaritinga, São Paulo, Brazil, 14 Apr. 2000, coll. R.J.F. Feres; 2 females collected on H. brasiliensis from São José do Rio Preto, São Paulo, Brazil, 01 Jul. 2003, coll. R.J.F. Feres (DZSJRP n. 10152–10154); 5 females collected on H. brasiliensis from Goianésia, Goiás, Brazil, 05 Dec. 2000, coll. R.J.F. Feres (DZSJRP n. 10155–10157); and 1 male, 3 deutonymphs, 1 protonymph and 3 larvae collected on H. brasiliensis from São José do Rio Preto, São Paulo, Brazil, 09 Jul. 2015, coll. E.B. Castro (DZSJRP n. 10706–10708).

Remarks — Baker (1945) and Baker & Pritchard (1953) did not mention the number of specimens used in the description and redescription of the species. Four type specimens were located, and these were remounted by USNM staff due to their poor condition. Now there are four slides, each with 1 female specimen (see above for deposition details). One of the paratypes was donated to Collection of Acari DZSJRP.

Redescription

Female (Figures 1-10; n=4) — Body measurements: distance between setae v2-h1 240 (230 – 250), sc2-sc2 150 (145 – 150); other measurements: v2-v2 32 (30 – 31), sc1-sc1 100 (95 – 105), c1-c1 25 (20 – 25), c3-c3 175 (165 – 175), d1-d1 7 (5 – 10), d3-d3 135 (130 – 145), e1-e1 6 (3 – 7), e3-e3 100 (85 – 112), f2-f2 82 (80 – 97), f3-f3 75 (72 – 75), h2-h2 60 (50 – 62), h1-h1 27 (22 – 27).

Dorsum (Figures 1-4) — Anterior margin of prodorsum with a pair of median triangular projections forming a notch. Dorsum completely ornamented; under SEM appears as fine narrow bands of elongate cells and fine reticulation (Fig. 2a); under DIC appears as: prodorsum – a series of fine oblique bands laterally, separated by small fine irregular unjoined cells; opisthosoma – a series of fine transverse bands centrally, separated by small fine irregular open cells (Fig. 1); triangular to semicircular plate weakly evident encompassing c3-d3. Dorsal setae v2, c1, d1, d3 and e1 short to minute; sc1, sc2, c3, e3, f2, f3, h1 ovate to lanceolate, barbed; h2 elongate and flagelliform. Setal lengths: v2 5 (4 – 5), sc1 10 (9 – 10), sc2 20 (20 – 23), c1 4 (3 – 4), c3 19 (16 – 19), d1 4 (3 – 4), d3 4 (4), e1 4 (4), e3 16 (17 – 20), f2 16 (13 – 18), f3 15 (14 – 17), h1 14 (10 – 14), h2 120 (100 – 125). Microplates: microplate layer consisting of a smooth base layer of tiny rounded wax-like crystals forming an even coating over the body, interspersed with large, individual, globular, conglomerate masses (Fig. 3).

Figure 1. Tenuipalpus heveae Baker (Female): dorsum.

Figure 2. Low-Temperature Scanning Electron Microscopy (LT-SEM) image of Tenuipalpus heveae Baker (Female): a – dorsal view; b – lateral view.

Figure 3. LT-SEM image of Tenuipalpus heveae Baker (Female): detail of microplates on integument of dorsum (15,000X magnification).

Figure 4. Differential interference contrast (DIC) image of Tenuipalpus heveae Baker (female paratype): dorsum.

Venter (Figures 5 and 7) — Ventral integument with fine, mostly longitudinal striae; with oblique striations becoming longitudinal near 3a setae; prodorsum with lateral margin longitudinally striate; with narrow band of transverse striae between setae 4a-4a and longitudinal striae 4a-ag; with broken transverse striae between ag and g1-g2; large region of smooth cuticle laterad setae 4a-ag. Striae surrounding coxae I and II longitudinal; striae surrounding coxae III and IV oblique to longitudinal. Coxal setae 1b and 2b smooth, other coxal setae sparsely plumose; setae 1a and 4a setae elongate and flagelliform; setae 3a smooth; setae ag, g1-2 and ps2-3 sparsely plumose. Setal lengths: 1a 70 (40 – 70), 1b 10 (10 – 11), 1c 14 (12 – 15), 2b 16 (12 – 20), 2c 21 (18 – 24), 3a 12 (10 – 12), 3b 20 (15 – 20), 4a 70 (70 – 75), 4b 17 (17 – 21), ag 17 (16 – 18), g1 16 (16 – 19), g2 19 (17 – 20), ps2 13 (12 – 16), ps3 14 (12 – 16).

Figure 5. Tenuipalpus heveae Baker (Female): venter.

Figure 6. Tenuipalpus heveae Baker (Female): ventral infracapitulum.

Figure 7. LT-SEM image of Tenuipalpus heveae Baker (Female): a – anterior ventral opisthosoma; b – posterior ventral opisthosoma.

Gnathosoma (Figures 6, 8-9) — Palps 3-segmented, second segment elongate bearing 1 long, barbed seta d 10 (9 – 13); third segment small with 1 eupathidium ul' 8 (7 – 8). Ventral setae m 11 (10 – 12), sparsely plumose; distance between setae m-m 15 (12 – 14). Tips of cheliceral stylets laterally serrated (Figure 9).

Figure 8. LT-SEM image of Tenuipalpus heveae Baker (Female): a – view of ventral infracapitulum, detail of protracted paired cheliceral stylets; b – detail of palp.

Figure 9. LT-SEM image of Tenuipalpus heveae Baker (Female): view of apex of chelicerae.

Legs (Figure 10) — Setal counts (from coxae to tarsi): I 2-1-4-1-5-9(1), II 2-1-4-1-5-9(1), III 1-1-2-0-2-4, IV 1-1-1-0-2-4. Setae d on femora I and II in dorsal position, not lateral; setae l' on trochanter III absent; setae d absent on tibiae III and IV; setae tc' absent on tarsi III – IV; seta ft" on tarsi I and II short, broadly lanceolate, barbed; tarsi I and II each with 1 short solenidion ω" [tarsi I 4 (4 – 5) and tarsi II 3 (3 – 4) respectively] and 2 eupathidia p' and p" (7 – 8, 7 – 8 for both tarsi I and tarsi II). Ventral setae on trochanters, femora, and tibiae I – IV sparsely plumose. See details of the development of leg chaetotaxy in Table 1.

Figure 10. Tenuipalpus heveae Baker (Female), dorsal aspect, right side, of: a – leg I; b – leg II; c – leg III; d – leg IV.

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-vermelho-da-seringueira".

Male (Figures 11-13; n=1) — Body measurements: distance between setae v2-h1 180, sc2-sc2 125; other measurements: v2-v2 33, sc1-sc1 80, c1-c1 25, c3-c3 125, d1-d1 13, d3-d3 100, e1-e1 8, e3-e3 70, f2-f2 70, f3-f3 60, h2-h2 50, h1-h1 20.

Dorsum (Figures 11-12) — Anterior margin of prodorsum with a pair of median triangular projections forming a notch. Dorsal cuticle mostly smooth. Prodorsum with weak oblique striae converging from sc1 to median sejugal furrow; semicircular plate weakly evident encompassing c3-d3. Dorsal setae v2, c1, d1, d3 and e1 short to minute; sc1, sc2, c3, e3, f2, f3, h1 lanceolate, barbed; h2 elongate and flagelliform. Setal lengths: v2 5, sc1 10, sc2 14, c1 6, c3 9, d1 6, d3 5, e1 5, e3 11, f2 12, f3 12, h1 10, h2 65.

Figure 11. Tenuipalpus heveae Baker (Male): dorsum.

Figure 12. Differential interference contrast (DIC) image of Tenuipalpus heveae Baker (Male): dorsum.

Venter (Figure 13a) — Ventral integument with fine striae; prodorsum with lateral margin longitudinally striate and with converging oblique striations surrounding 3a setae; with broken transverse striae between setae 4a and g1-g2. Striae on coxae I-IV oblique to longitudinal. Coxal setae 1b and 2b smooth, other coxal setae sparsely plumose; setae 1a and 4a setae elongate and flagelliform; setae 3a, ag and ps2 smooth; setae g1-2 sparsely plumose. Setae ps3 modified and inserted in a distal position in the anal valves. Setal lengths: 1a 65, 1b 10, 1c 12, 2b 13, 2c 16, 3a 11, 3b 16, 4a 65, 4b 14, ag 13, g1 14, g2 15, ps2 12, ps3 11.

Figure 13. Tenuipalpus heveae Baker (Male): a – venter. Note seta g2 missing on the right side; b – aedeagus.

Gnathosoma — Palps similar to those of female. Tibial seta d 8, tarsal eupathidium ul' 7. Ventral setae m 9; distance between setae m-m 12.

Legs — Same setal distribution as female; tarsi I and II each with 1 solenidion ω" [tarsi I 5 and tarsi II 6, respectively], ω' absent, and 2 eupathidia p' and p" (tarsi I 6 and tarsi II 7, respectively).

Aedeagus (Figure 13b) — As figured; 82 long.

Deutonymph (n=3) — Body size measurements: distance between setae v2-h1 220 – 235, sc2-sc2 122 – 125; other measurements: v2-v2 25 – 28, sc1-sc1 82 – 90, c1-c1 23, c3-c3 145 – 150, d1-d1 10 – 13, d3-d3 115 – 120, e1-e1 5 – 8, e3-e3 82 – 85, f2-f2 72 – 78, f3-f3 65 – 70, h2-h2 35 – 38, h1-h1 12 – 15.

Dorsum (Figures 14-15a) — Anterior margin of prodorsum with a pair of small triangular projections forming a short, broad notch. Prodorsum with anterior central region smooth; region between setae sc2 and d1 with widely spaced transverse folds becoming oblique laterally; region posterior to d1-c3 smooth. Dorsal setae mostly similar in shape to adults, except narrower and setae sc2 longer – v2, c1, d1, d3, and e1 minute; sc2 long, narrow; sc1, c3, e3, f2, f3, h1 lanceolate to weakly falcate; h2 elongate, flagelliform. Setal lengths: v2 3 – 4, sc1 13 – 15, sc2 30 – 31, c1 3 – 4, c3 15 – 17, d1 2 – 3, d3 3, e1 3 – 4, e3 17 – 19, f2 15 – 17, f3 14 – 15, h1 9 – 11, h2 55 – 80.

Figure 14. Tenuipalpus heveae Baker (Deutonymph): dorsal habitus.

Figure 15. LT-SEM image of Tenuipalpus heveae Baker (Deutonymph): a – dorsal view; b – lateral view of legs I and II.

Venter — Ventral integument covered with fine transverse striae, weak between setae 3a and 4a. Setal lengths: 1a 55 – 60, 1b 7 – 8, 1c 7 – 9, 2b 8 – 9, 2c 10 – 12, 3a 9 – 10, 3b 9 – 11, 4a 35 – 50, 4b 7 – 8, ag 7 – 8, g1 7 – 8, ps2 5 – 6, ps3 6 – 7. Setae g2 absent.

Gnathosoma — Palps similar to those of adults. Tibial seta d 6 – 7, tarsal eupathidium ul' 6 – 7. Ventral seta m 6 – 7; distance between setae m-m 11 – 12.

Legs (Figure 15b) — Setal counts (from coxae to tarsi): I 2-1-4-1-5-9(1), II 2-1-4-1-5-9(1), III 1-1-2-0-2-4, IV 1-0-1-0-2-3. Setal additions: setae v' added to trochanters I-III; setae l' added to femora I-II; setae d added to genua I and II; setae tc'-tc" added to tarsi I-II; setae tc" added to tarsus III. Seta ft" on tarsi I and II short, broadly lanceolate, barbed; tarsi I and II each with 1 short solenidion ω" 3 (for both tarsi I and tarsi II) and 2 eupathidia p' and p" (all 6 long). See details of the development of leg chaetotaxy in Table 1.

Table 1. Ontogenetic development of leg setae of Tenuipalpus heveae (Th) and Tenuipalpus vieirae (Tv). Setae are indicated in the stage in which they first appear. Setae in parentheses represent pairs.

Protonymph (n=1) — Body size measurements: distance between setae v2-h1 178, sc2-sc2 98; other measurements: v2-v2 23, sc1-sc1 68, c1-c1 23, c3-c3 105, d1-d1 13, d3-d3 78, e1-e1 5, e3-e3 58, f2-f2 55, f3-f3 43, h2-h2 25, h1-h1 10.

Dorsum (Figure 16) — Anterior margin of prodorsum with a pair of small rounded projections, forming a shallow notch. Prodorsum with anterior central region smooth; region between setae sc2 and d1 with widely spaced transverse folds becoming oblique laterally; region posterior to setae d1-c3 smooth. Dorsal setae mostly similar in shape to deutonymph, except sc1, sc2, c3, c3, f2 and f3 slightly smaller. Setal lengths: v2 3, sc1 10, sc2 27, c1 2, c3 12, d1 2, d3 2, e1 3, e3 15, f2 12, f3 11, h1 8, h2 50.

Figure 16. Tenuipalpus heveae Baker (Protonymph): dorsal habitus.

Venter — Ventral integument covered with fine transverse striae. Setal lengths: 1a 40, 1b 7, 1c 7, 2c 7, 3a 8, 3b 7, ag 8, ps2 5, ps3 6. Setae 2b, 4a, 4b, g1 and g2 absent.

Gnathosoma — Palps similar to those of adults. Tibial seta d 5, tarsal eupathidium ul' 6. Ventral seta m 6; distance between setae m-m 10.

Legs — Setal counts (from coxae to tarsi): I 2-0-3-0-5-7(1), II 1-0-3-0-5-7(1), III 1-0-2-0-2-3, IV 0-0-1-0-2-3. Setal additions: 1c added to coxae I; 2c added to coxae II; 3b added to coxae III; setae l' absent on trochanter III. Tarsi I and II each with 1 solenidion ω" 3 (for both tarsi I and tarsi II) and 2 eupathidia p' and p" (5, 6, for both tarsi I and II).

Larva (n=3) — Body measurements: distance between setae v2-h1 145 – 157, sc2-sc2 70 – 85; other measurements: v2-v2 17 – 20, sc1-sc1 52 – 60, c1-c1 17 – 22, c3-c3 82 – 95, d1-d1 13, d3-d3 59 – 65, e1-e1 8, e3-e3 50 – 57, f2-f2 45 – 50, f3-f3 35 – 38, h2-h2 20 – 23, h1-h1 7 – 10.

Dorsum (Figure 17) — Anterior margin of prodorsum smoothly rounded, without median projections. Prodorsum with anterior margin colliculate; region between sc2 and d1-c3 with few transverse to oblique folds becoming oblique laterally; region posterior to setae d1 with broken longitudinal to oblique striations. Dorsal setae mostly similar in shape to protonymph, except sc1 and sc2 slightly smaller. Setal lengths: v2 2 – 3, sc1 6 – 7, sc2 19 – 20, c1 2, c3 11 – 12, d1 2 – 3, d3 2, e1 2 – 3, e3 13 – 16, f2 14, f3 12 – 13, h1 9 – 10, h2 45 – 55.

Figure 17. Tenuipalpus heveae Baker (Larva): dorsal habitus.

Venter — Ventral integument with fine irregular striae. Setal lengths: 1a 35 – 50, 1b 5 – 6, 3a 6 – 9, ps2 5 – 6, ps3 4 – 6. As is normal for tenuipalpids, setae 1c, 2b, 2c, 3b, 4a, 4b, ag, g1 and g2 absent.

Gnathosoma — Palps similar to that of adults. Tibial seta d 5 – 6, tarsal eupathidium ul' 4 – 5. Ventral setae m absent.

Legs — Setal counts (from coxae to tarsi): I 1-0-3-0-5-7(1), II 0-0-3-0-5-7(1), III 0-0-2-0-2-3; setae d absent on tibia III. Tarsi I and II each with 1 solenidion ω" 2 (for both tarsi I and tarsi II) and eupathidia p' and p" (4, 5; 4, 5 respectively). All legs covered with colliculate sculpturing.

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.

Table 2. Measurements of the body and dorsal setae for type and non-type females of Tenuipalpus heveae Baker. Measurements for the holotype with range for the paratypes are shown in parentheses.
Tenuipalpus vieirae n. sp. Castro, Ramos and Feres

Figures (18-25)

ZOOBANK: 3F539E51-5C3E-470F-B6DE-C63FE8AEACC8

Diagnosis — Female: Dorsum completely smooth; triangular to semicircular plate evident encompassing c3-d3. Anterior margin of prodorsum with pair median triangular projections, forming a notch. Dorsum with setae v2, sc1, c1, c3, d1, d3, e1, e3 minute to short; setae sc2 narrowly lanceolate, barbed; setae f2, f3 and h1 lanceolate to ovate, barbed, much broader than other dorsal setae; setae h2 elongate, flagelliform. Palps three segmented. Ventral integument with regions of smooth cuticle and with regions of finely striate cuticle; transverse to oblique striations between setae 1a and 3a; ventral prodorsum with lateral margin longitudinally striate; striae surrounding coxae III and IV oblique; large region of smooth cuticle laterad 4a-ps setae; fine transverse striae between setae ag and g1-g2. Coxal setae 1b and 2b filiform and smooth, other coxal setae sparsely plumose. Tarsi I – IV 9(1)-9(1)-4-4 (setae tc' absent on tarsus III and IV); trochanters I-IV 1-1-2-1 (seta l' present on trochanter III); setae d present on tibia III but absent on tibia IV. Immatures: most dorsal setae are similar to those of the female.

Type material examined — Holotype: female collected on Hevea brasiliensis Muell Arg. (Euphorbiaceae) from Manaus, Amazonas, Brazil, 21 Dec. 2000, coll. T.J. Izzo, deposited in Acari Collection, Departamento de Zoologia e Botânica, UNESP, located at the São José do Rio Preto, State of São Paulo, Brazil (DZSJRP no. 10158). Paratypes: 5 females, 1 deutonymph, 2 protonymphs and 2 larvae with the same data as that of the holotype (DZSJRP nos. 10159–10164); 3 females, 1 deutonymph and 1 larva collected on H. guianensis Aubl. (Euphorbiaceae) from Manaus, Amazonas, Brazil, Aug. 2012, coll. F.M. Nuvoloni (DZSJRP no. 10165, USNM).

Description

Female (Figures 18-22, n=9) — Body measurements: distance between setae v2-h1 232 (210 – 237), sc2-sc2 135 (120 – 142); other measurements: v2-v2 30 (27 – 30), sc1-sc1 75 (72 – 77), c1-c1 22 (17 – 27), c3-c3 162 (152 – 167), d1-d1 10 (10 – 12), d3-d3 142 (130 – 142), e1-e1 7 (5 – 10), e3-e3 97 (82 – 102), f2-f2 95 (80 – 97), f3-f3 77 (67 – 80), h2-h2 62 (37 – 62), h1-h1 17 (15 – 22).

Dorsum (Figures 18-19) — Anterior margin of prodorsum with a pair of median triangular projections forming a notch. Dorsum completely smooth; triangular to semicircular plate encompassing setae c3-d3 weakly evident. Dorsal setae v2, sc1, c1, c3, d1, d3, e1, e3 minute to short; setae sc2 narrowly lanceolate and barbed; setae f2, f3 and h1 lanceolate to ovate, barbed, much broader than other dorsal setae; setae e3 distinctly smaller than setae f2 and f3; h2 elongate, flagelliform. Setal lengths: v2 4 (2 – 4), sc1 4 (2 – 5), sc2 15 (15 – 31), c1 4 (3 – 4), c3 6 (4 – 6), d1 4 (2 – 4), d3 5 (2 – 5), e1 broken (1 – 4), e3 5 (5 – 9), f2 13 (13 – 16), f3 14 (12 – 18), h1 12 (8 – 12), h2 120 (95 – 120).

Figure 18. Tenuipalpus vieirae n. sp. (Female): dorsum.

Figure 19. DIC image of Tenuipalpus vieirae n. sp. (Female): dorsum.

Venter (Figure 20) — Ventral integument with regions of smooth cuticle and regions of finely striate cuticle; transverse to oblique striations between setae 1a and 3a; ventral prodorsum with lateral margin longitudinally striate. Striae surrounding coxae I and II longitudinal; striae surrounding coxae III and IV oblique; large region of smooth cuticle laterad setae 4a-ps setae; fine transverse striae between ag and g1-g2. Coxal setae 1b and 2b filiform and smooth, other coxal setae sparsely plumose; setae 1a and 4a elongate and flagelliform; seta 3a smooth; setae ag, g1-2 and ps2-3 sparsely plumose. Setal lengths: 1a broken (65 – 80), 1b 7 (5 – 11), 1c 15 (10 – 17), 2b 11 (10 – 13), 2c 20 (16 – 24), 3a 10 (9 – 10), 3b 15 (12 – 22), 4a 90 (60 – 95), 4b 18 (13 – 20), ag 21 (14 – 21), g1 17 (15 – 21), g2 17 (14 – 17), ps2 20 (13 – 20), ps3 15 (10 – 15).

Figure 20. Tenuipalpus vieirae n. sp. (Female): venter.

Gnathosoma (Figure 21) — Palps 3-segmented, second segment elongate bearing long, barbed d seta 10 (7 – 12); third segment small with 1 eupathidium ul' 7 (5 – 7). Ventral setae m 9 (5 – 9), sparsely plumose; distance between setae m-m 14 (11 – 14).

Figure 21. Tenuipalpus vieirae n. sp. (Female): ventral infracapitulum.

Legs (Figure 22) — Setal counts (from coxae to tarsi): I 2-1-4-1-5-9(1), II 2-1-4-1-5-9(1), III 1-2-2-0-3-4, IV 1-1-1-0-2-4. Setal additions: only two setae are added to the legs in the adult female, v' is added to trochanter IV and tc" is added to tarsus IV. Setae d in distinctly dorsal position on femora I – II; seta d present on genua I and II; seta d present on tibia III and absent on tibiae IV; seta tc' absent on tarsi III and IV. Seta ft" on tarsi I and II short, broadly lanceolate, barbed; tarsi I and II each with 1 short solenidion ω" 4 (3 – 4) (for both tarsi I and tarsi II) and 2 eupathidia p' and p" (5 – 6, 4 – 7 for both tarsi). Ventral setae on trochanters, femora and tibiae sparsely plumose. See details of the development of leg chaetotaxy in Table 1.

Figure 22. Tenuipalpus vieirae n. sp. (Female), dorsal aspect, right side, of: a – leg I; b – leg II; c – leg III; d – leg IV.

Color — The body is dark red with some black spots. The legs are red. Leg and dorsal setae are orange.

Male — Unknown.

Deutonymph (n=2) — Body size measurements: distance between setae v2-h1 217 – 235, sc2-sc2 105 – 130; other measurements: v2-v2 25 – 27, sc1-sc1 75 – 80, c1-c1 22, c3-c3 142 – 160, d1-d1 10 – 12, d3-d3 107 – 122, e1-e1 2 -5, e3-e3 70 – 87, f2-f2 65 – 80, f3-f3 52 – 62, h2-h2 32 – 40, h1-h1 12 – 15.

Dorsum (Figure 23) — Anterior margin of prodorsum with a pair of small rounded projections, forming a shallow notch. Prodorsum with anterior central region smooth; region between setae sc2 and d1 with widely spaced transverse folds becoming oblique laterally; region posterior to d1-c3 smooth. Dorsal setae mostly similar in shape to adult female, except setae sc2, c3 and e3 of different size – v2, sc1, c1, d1, e1 minute; sc2 long, narrow; c3, e3, f2, f3, h1 lanceolate to weakly falcate; h2 elongate, flagelliform. Setal lengths: v2 2, sc1 3, sc2 36 – 37, c1 3 – 4, c3 8 – 14, d1 3, d3 2, e1 2, e3 12 – 15, f2 15 – 16, f3 15 – 17, h1 7 – 10, h2 70 – 110.

Figure 23. Tenuipalpus vieirae n. sp. (Deutonymph): dorsal habitus.

Venter — Ventral integument covered with fine transverse striae, weakly between setae 3a and 4a. Setal lengths: 1a 75, 1b 5, 1c 5 – 9, 2b 4, 2c 8 – 9, 3a 7 – 9, 3b 5 – 7, 4a 35 – 45, 4b 5 – 6, ag 6 – 8, g1 5 – 6, ps2 5 – 6, ps3 4. Setae g2 absent.

Gnathosoma — Palps similar to those of adults. Tibial seta d 5 – 6, tarsal eupathidium ul' 5. Ventral seta m 5 – 6; distance between setae m-m 5 – 11.

Legs — Setal counts (from coxae to tarsi): I 2-1-4-1-5-9(1), II 2-1-4-1-5-9(1), III 1-2-2-0-3-4, IV 1-0-1-0-2-3. Setal additions: setae v' added to trochanters I-III; setae l' added to femora I-II; setae d added to genua I and II; setae tc'-tc" added to tarsi I-II; setae tc" added to tarsus III. Seta ft" on tarsi I and II short, broadly lanceolate, barbed; tarsi I and II each with 1 short solenidion ω" (tarsi I 2 – 3 and tarsi II 3) and eupathidia p' and p" (5, 5 – 6; 5, 5 respectively). See details of the development of leg chaetotaxy in Table 1.

Protonymph (n=2) — Body size measurements: distance between setae v2-h1 174 – 176, sc2-sc2 103 – 108; other measurements: v2-v2 21 – 23, sc1-sc1 65 – 67, c1-c1 20, c3-c3 120 – 124, d1-d1 9 – 11, d3-d3 91 – 95, e1-e1 4 – 5, e3-e3 69 – 72, f2-f2 61 – 63, f3-f3 45 – 48, h2-h2 28 – 31, h1-h1 10.

Dorsum (Figure 24) — Anterior margin of prodorsum with a pair of small rounded projections, forming a shallow notch. Prodorsum with anterior central region smooth; region between setae sc2 and d1 with widely spaced transverse folds becoming oblique laterally; region posterior to setae d1-c3 smooth. Dorsal setae mostly similar in shape to deutonymph, except c1, d1 thicker and more barbed; dorsal setae similar in shape to larva, except c1, d1, e1 smaller. Setal lengths: v2 2, sc1 2, sc2 28 – 32, c1 3 – 4, c3 10, d1 3 – 5, d3 1 – 2, e1 2 – 3, e3 12 – 14, f2 17 – 19, f3 17 – 20, h1 5 – 10, h2 40 – 45.

Figure 24. Tenuipalpus vieirae n. sp. (Protonymph): dorsal habitus.

Venter — Ventral integument covered with fine transverse striae. Setal lengths: 1a 55, 1b 4 – 5, 1c 4 – 5, 2c 6 – 7, 3a 5, 3b 6 – 8, ag 5 – 6, ps2 5, ps3 3. Setae 2b, 4a, 4b, g1 and g2 absent.

Gnathosoma — Palps similar to those of adults. Tibial seta d 5, tarsal eupathidium ul' 3 – 4. Ventral seta m 4 – 5; distance between setae m-m 9 – 10.

Legs — Setal counts (from coxae to tarsi): I 2-0-3-0-5-7(1), II 1-0-3-0-5-7(1), III 1-1-2-0-3-3, IV 0-0-1-0-2-3. Setal additions: 1c added to coxae I; 2c added to coxae II; 3b added to coxae III; l' added to trochanter III. Tarsi I and II each with 1 solenidion ω" (tarsi I 2-3 and tarsi II 2) and 2 eupathidia p' and p" (5, 5, for both tarsi I and II).

Larva (n=3) — Body measurements: distance between setae v2-h1 138-150, sc2-sc2 75-82; other measurements: v2-v2 16 – 17, sc1-sc1 59-60, c1-c1 21 – 24, c3-c3 79 – 94, d1-d1 10 – 13, d3-d3 53 – 65, e1-e1 4, e3-e3 53 – 55, f2-f2 45 – 47, f3-f3 31 – 35, h2-h2 12 – 18, h1-h1 5 – 8.

Dorsum (Figure 25) — Anterior margin of prodorsum smoothly rounded, without median projections. Prodorsum with anterior central region colliculate; region between sc2 and d1-c3 with transverse to oblique folds becoming oblique laterally; region posterior to setae d1 with longitudinal to oblique striations. Dorsal setae mostly similar in shape to protonymph, except c1, d1 slightly larger. Setal lengths: v2 1 – 2, sc1 1 – 2, sc2 20, c1 6 – 7, c3 7 – 12, d1 7, d3 1, e1 4, e3 11 – 12, f2 13 – 14, f3 11 – 12, h1 9, h2 37 – 40.

Figure 25. Tenuipalpus vieirae n. sp. (Larva): dorsal habitus.

Venter — Ventral integument with fine irregular striae. Setal lengths: 1a 20, 1b 4, 3a 4 – 6, ps2 1 – 2, ps3 1. As is normal for tenuipalpids, setae 1c, 2b, 2c, 3b, 4a, 4b, ag, g1 and g2 absent.

Gnathosoma — Palps similar to that of adults. Tibial seta d 6, tarsal eupathidium ul' 4. Ventral setae m absent.

Legs — Setal counts (from coxae to tarsi): I 1-0-3-0-5-7(1), II 0-0-3-0-5-7(1), III 0-0-2-0-3-3. Chaetotaxy: setae l' absent on genua I-III; setae d present on tibia III. Tarsi I and II each with 1 solenidion ω" 2 (for both tarsi I and tarsi II) and eupathidia p' and p" (4, 5; 5, 5 respectively). All legs covered with colliculate sculpturing.

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.

Besides T. heveae, four other Brazilian species of Tenuipalpus were described from Euphorbiaceae plants (T. moraesi Feres & Hernandes (2006), T. isabelae Mesa, Moraes & Ochoa (2006), T. tapiae De Castro & Feres (2013) and T. toropi Castro, Ramos & Feres (2015)), but none of them were collected on the same host plant species as T. vieirae n. sp.. Furthermore, T. vieirae is readily differentiated from these four species by the dorsum being completely smooth.

The new species also resembles Tenuipalpus zanthus De Leon, 1965 because both species have a smooth dorsum. We examined the types and found that, in addition to a few other characters listed below, the chaetotaxy of the genua, tibiae and tarsi are different between these two species: genua 1-1-0-0 in T. vieirae n. sp. and 3-3-1-0 in T. zanthus; tibia 5-5-3-2 in T. vieirae n. sp. and 5-5-3-3 in T. zanthus and; tarsi 9(1)-9(1)-4-4 in T. vieirae n. sp. and 9(1)-9(1)-5-5 in T. zanthus. Tenuipalpus zanthus is recorded as being pale green (De Leon 1965), and it is a larger mite also, being 250 – 265 long (v2-h1) and 155 – 165 wide (sc2-sc2), while T. vieirae is 210 – 237 long (v2-h1) and 120 – 142 wide (sc2-sc2).

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.

Acknowledgements

We thank to Dr. Gregory Evans (APHIS – USDA) and Dr. Gilberto J. de Moraes (ESALQ-USP) for the revision of the manuscript; to Dr. Carlos H.W. Flechtmann (ESALQ-USP) by his help with the bibliography; to Chris Pooley (ECMU-USDA) for his help with the micrographs. To Drs. Jennifer J. Beard (Queensland Museum, Australia) and Cal Welbourn (Florida Department of Agriculture and Consumer Services) for their valuable suggestions and comments on the manuscript. Part of the studied specimens of T. heveae and of the new species described was collected with financial support of the "Fundação de Amparo à Pesquisa do Estado de São Paulo" (FAPESP) (Proc. n° 2010/19935-1). This work was supported by the "Coordenação de Aperfeiçoamento de Pessoal de Nível Superior" (CAPES) (Proc. BEX 7768/13-3) and "Fundação de Amparo à Pesquisa do Estado de São Paulo" (FAPESP) (Proc. 2016/01193-5) by fellowship to the first author and by the "Conselho Nacional de Desenvolvimento Científico e Tecnológico" (CNPq) (Proc. 303435/2013-5) by research grant to the third author. To the Smithsonian Natural History Museum and National Agricultural Library (NAL-USDA), SEL-USDA for support and assistance with specimens and references. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA; USDA is an equal opportunity provider and employer.

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Article editorial history

Date received:
2016-05-13
Date accepted:
2016-10-31
Date published:
2017-04-20

Edited by:
Navia, Denise

(CC BY 4.0)
© 2017 Castro, Elizeu B.; Ramos, Felipe A.M.; Feres, Reinaldo J.F.; Ochoa, Ronald and Bauchan, Gary R.

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