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Research Article
New species of Daidalotarsonemus and Excelsotarsonemus (Acari, Tarsonemidae) from the Brazilian rainforest
expand article infoJosé Marcos Rezende‡, Antonio Carlos Lofego§, Ron Ochoa|, Gary Bauchan
‡ PPG Biologia Animal, UNESP - Universidade Estadual Paulista, São José do Rio Preto, Brazil
§ UNESP-Universidade Estadual Paulista, São José do Rio Preto, Brazil
| USDA, SEL, ARS, Beltsville, Maryland, United States of America
¶ USDA-ARS, Beltsville, United States of America

Corresponding author: José Marcos Rezende ( jmrezende@live.com )

Academic editor: Vladimir Pesic
© 2015 José Marcos Rezende, Antonio Carlos Lofego, Ron Ochoa, Gary Bauchan.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Rezende JM, Lofego AC, Ochoa R, Bauchan G (2015) New species of Daidalotarsonemus and Excelsotarsonemus (Acari, Tarsonemidae) from the Brazilian rainforest. ZooKeys 475: 1-36. https://doi.org/10.3897/zookeys.475.8827
ZooBank: urn:lsid:zoobank.org:pub:664344E4-FA3F-4F12-A1EE-83B95BFE09AF
Open Access

Abstract

Three new species of Tarsonemidae, Daidalotarsonemus oliveirai Rezende, Lofego & Ochoa, sp. n., Excelsotarsonemus caravelis Rezende, Lofego & Ochoa, sp. n. and Excelsotarsonemus tupi Rezende, Lofego & Ochoa, sp. n. are described and illustrated. Measurements for these species are provided, as well as drawings, phase contrast (PC), differential interference contrast (DIC) and low temperature scanning electron microscopy (LT-SEM) micrographs. Some characters, which have not been used or clearly understood, are described herein. Biological, ecological and agricultural aspects about the role of these species in the rainforest and its surrounding environment are briefly discussed.

Keywords

Atlantic Forest, canopy, faunistics, LT-SEM, systematics, Tarsonemoidea , Trombidiformes

Introduction

Currently, Daidalotarsonemus De Leon (Acari, Prostigmata, Tarsonemidae) consists of 26 described species (Lin and Zhang 2002, Lofego et al. 2005, Sousa et al. 2014). It is one of the few genera of Tarsonemidae which have been documented on all continents, except Antarctica (Lindquist 1986, Lin and Zhang 2002). The known geographical distribution of Excelsotarsonemus Ochoa & Naskręcki is much more restricted, previously recorded only from Costa Rica. The two genera are closely related and considered to be sister genera (Ochoa et al. 1995, Ochoa and OConnor 1998). Both are considered to be plant inhabiting taxa, apparently with a preference for plants located in humid places, where there is an abundance of fungi, bacteria and lichens. In Brazil, the Amazon and Atlantic Rainforests are biomes which fit these requirements, because of their high temperature and rainfall index.

In recent years, significant advances in microscopy have expanded our knowledge of the morphological characters of organisms, which has led to a better understanding of the taxonomy and ecology of species (Fisher and Dowling 2010). One of most effective techniques that has been integrated to study mite morphology and biology is Low Temperature Scanning Electron Microscopy (LT-SEM), in which a sample is instantly frozen with liquid nitrogen, making a frozen snap-shot of the specimen as it occurs in nature available for microscopic study (Bolton et al. 2014). This procedure is critical for understanding not only external morphology, but also ecological and behavior characteristics, not accessible using light microscopy.

The objective here is to describe new species of Daidalotarsonemus and Excelsotarsonemus found in a rainforest in Brazil using phase contrast (PC), differential interference contrast (DIC) light microscopy and LT-SEM microscopy techniques. The LT-SEM study led to a better understanding of the morphology of these species and their respective genera and is discussed herein.

Material and methods

Several leaves of Annona muricata L. (Annonaceae), Theobroma cacao L. (Malvaceae) and Spondias purpurea L. (Anacardiaceae) were collected in and the area surrounding a section of the rainforest near Santa Cruz State University campus (UESC), 14°47'45"S; 39°10'18"W, Ilhéus, Bahia State, Brazil. The region is characterized by having high relative humidity (75–90%) and high precipitation (100–330 mm/month) indexes throughout the year. Mites collected in the study were prepared and analysed using three different microscopy techniques: phase contrast (PC), differential interference contrast (DIC) and low temperature scanning electron microscopy (LT-SEM). The terminology used herein follows that of Lindquist (1986), except fot the gnathosomal setae dgs and vgs (Magowski and Di Palma 2000). For each structure, all the measurements are provided in micrometers (µm), followed by the range of all specimens measured in parentheses, including the holotype. The following abbreviations are used for institutions where the types were deposited: Acari Collection of the Departamento de Zoologia e Botânica (DZSJRP), São Paulo State University, São José do Rio Preto, São Paulo, Brazil; United States National Museum of Natural History (USNM), Smithsonian Institution, housed in Beltsville, Maryland 20705, USA.

Specimens were prepared and observed with an LT-SEM using the same techniques as described in Bolton et al. (2014). Briefly, live specimens were secured to 15 cm × 30 cm copper plates using ultra smooth, round (12 mm diameter), carbon adhesive tabs (Electron Microscopy Sciences, Inc., Hatfield, PA). The specimens were frozen in a Styrofoam box, by placing the plates on the surface of a pre-cooled (-196 °C) brass bar whose lower half was submerged in liquid nitrogen (LN2). After 20–30 seconds, the holders containing the frozen samples were transferred the Quorum PP2000 cryo-prep chamber (Quorum Technologies, East Sussex, UK) attached to an S-4700 field emission scanning electron microscope (Hitachi High Technologies America, Inc., Dallas, TX). The specimens were etched inside the cryotransfer system to remove any surface contamination (condensed water vapour) by raising the temperature of the stage to -90 °C for 10–15 minutes. Following etching, the temperature inside the chamber was lowered below -130 °C, and the specimens were coated with a 10 nm layer of platinum using a magnetron sputter head equipped with a platinum target. The specimens were transferred to a pre-cooled (-130 °C) cryostage in the SEM for observation. An accelerating voltage of 5 kV was used to view the specimens. Images were captured using a 4pi Analysis System (Durham, NC). For the PC and DIC micrographs, it was used a Zeiss Axioscope™ microscope with differential interference contrast (DIC) 100× Plan Apochromatic objective with a NA 1.4. For the drawings, it was used a Leica® DM 2500 microscope with a drawing tube attached. Images were sized and placed together to produce a single illustrative plate using the software Adobe® Photoshop CS 5.0 and Adobe® Illustrator CS 5.0.

Results

Daidalotarsonemus oliveirai Rezende, Lofego & Ochoa, sp. n.

http://zoobank.org/4929C981-2DE8-4145-9C2F-6FBF54B92F67
Figs 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14

Diagnosis

Females of the new species are most similar to those of Daidalotarsonemus jamesbakeri Smiley (1969) and D. folisetae Lofego & Ochoa (Lofego et al. 2005), because of the irregular ornamentation pattern on the prodorsum and the similar shape of the setae e. However, Daidalotarsonemus oliveirai sp. n. has the tergite C with a W-shaped reticulate pattern in central area and longitudinal, wavy interrupted ridges laterally, whereas in D. jamesbakeri and D. folisetae the reticulation is uniform on all tergites, with longitudinal continuous ridges. The shape of setae e is also different among the three species, being cordate in D. oliveirai, acicular in D. jamesbakeri, and phylliform in D. folisetae. Males are similar to Daidalotarsonemus deleoni Smiley (1967), by the shape and length of almost all dorsal setae, except the setae sc1. In D. oliveirai, the relative length of the setae sc1/sc2 is 1:0.6, whereas in D. deleoni is 1:0.3.

Adult female

(6 specimens measured). Gnathosoma (Figs 3 and 6): partially covered by the prodorsum. Subtriangular in ventral view, length 24 (23–26), maximum width 21 (19–23); dorsal apodeme distinct. Setae dgs 9 (8–10) and vgs 6 (6) smooth; palps moderately long 9 (8–11), with two small subterminal setae and terminal projections. Pharynx fusiform, 19 (18–23) long and 6 (5–7) wide at maximum width. Gnathosoma, idiosoma and legs covered with tiny dimples, each around 0.3 (0.2–0.5) in diameter.

Idiosoma – dorsum (Figs 1–2): length 179 (170–188), width at level of c1 82 (75–90); prodorsal shield with irregular ornamentation covers the gnathosoma. Entire dorsum covered with cerotegument (Fig. 2C). Stigma located near lateral notch of prodorsal shield, which is equidistant to the v1 and sc2 setal bases. Tergite C with a W-shaped reticulate pattern in central area and longitudinal, wavy uninterupted ridges laterally; tergite D ornamented with regular sculpturing. Lengths of the setae: v1 23 (22–25), sc1 11 (10–12) (Fig. 7C), sc2 28, c1 11 (10–12), c2 11 (10–12), d 33 (31–35), e 15 (15–16), f 24 (23–25) and h 24 (24–25). Maximum width of expanded setae: d 6 (5–7), e 15 (14–16) and f 7 (7–8). All dorsal setae serrate, except for c2 smooth. Bothridial setae sc1 capitate, with tiny spines. Setae v1, sc2, c1, c2 and h setiform; setae d, e and f inserted on tubercles (Fig. 7D-E). Setae d linear and e cordate, both with a central serrate vein; f lanceolate, with two serrate veins. Distances between dorsal setae: v1–v1 25 (24–27), sc2–sc2 46 (44–48), v1–sc2 23 (23–24), c1–c1 50 (49–53), c2–c2 82 (76–88), c1–c2 27, d–d 44 (40–48), f–f 10, e–f 12 (11–13) and h–h 16 (14–17). Seta sc2 inserted anteriorly to sc1. Dorsal cupules not easily seen.

Idiosoma – venter (Figs 3–4): setae 1a 6 (6–7), posteriad of apodemes 1; 2a 9 (9), posterolaterad of apodemes 2; 3a 14 (13–15) near anteriomedial margins of apodemes 3; 3b 11 (11–12) on posterior margins of apodemes 4. Apodeme 1 conspicuous, fused to anterior end of prosternal apodeme. Apodeme 2 long and fused to the prosternal apodeme. Prosternal apodeme conspicuous from junction with apodeme 1 to the middle portion of sejugal apodeme. Sejugal apodeme uninterrupted, with a single median indentation. Apodeme 3 with a constriction near the anterior end, extending diagonally from proximity of base of seta 3a to anterior margin of trochanter III; apodeme 4 extending diagonally from the middle of the poststernal apodeme to base of seta 3b. Poststernal apodeme bifurcated anteriorly. Tegula wide 12 (11–13) and very short, 4 (4–5) (Fig. 7F); posterior margin slightly arched. Seta ps 12 (11–13) serrate. Ventral surface covered with tiny dimples (Fig. 7F).

Legs (Fig. 5): lengths (measured from femur to tarsus): leg I 40 (39–42), leg II 37 (35–40), leg III 79 (78–80). Number of setae (solenidia in parentheses) on femur, genu, tibia and tarsus, respectively: leg I: 3-4-5(2)-7(1), leg II: 3-3-4-4(1), leg III: 1+2-4-4. Claws medium-sized (not reduced) and hooked. Empodia of the legs I, II and III about the same size or slightly smaller compared to the respective basal stalks. Tarsal solenidion ω of tibiotarsus I 6 (5–7), stout, wider medially. Sensory cluster of tibia I complete (Fig. 7A), solenidion φ1 3 (3–4), slender, capitate; solenidion φ2 4, robust, slightly capitate; famulus k 6; all inserted at approximately the same level. Seta d of tibia I 18 (18–19), serrate. Solenidion ω of tarsus II proximally inserted, 4 long, stout, wider medially (Fig. 7B). Seta d of tibia II 13 (13–14), serrate. Femorogenu IV 11 (14–15); tibiotarsus IV 8. Length of leg IV setae: v’ F 9, v’ G 11, v´ Ti 19 and tc” 24 (23–27); setae v’ Ti and tc” serrate; v’ Ti falcate.

Adult male

(3 specimens measured). Gnathosoma (Figs 10, 13 and 14A): subtriangular in ventral view, length 22 (21–23), maximum width 20 (19–20); dorsal apodeme distinct. Setae dgs 11 (10–12) and vgs 7 (7) smooth; Palps moderately long 9 (8–10), with 2 small subterminal setae and terminal projections. Pharynx fusiform, 15 (14–17) long and 7 (6–8) wide at widest region. Gnathosoma, idiosoma and legs covered with tiny dimples, each 0.3 (0.2–0.5) in diameter.

Idiosoma – dorsum (Figs 8–9): length 174 (170–178), maximum width 82 (80–84). Prodorsal shield trapezoidal. Length of dorsal setae: v1 30 (29–31), v2 24 (22–25), sc1 38 (37–40), sc2 24 (22–25), c1 21 (20–22), c2 26 (24–29), d 32 (30–34), f 14 (13–16). All setae setiform and serrate. Distances between dorsal setae: v1–v1 13 (12–14), sc1–sc1 34 (32–35), sc2–sc2 44 (43–46), v1–sc2 26 (25–27), c1–c1 75 (74–77), c2–c2 78 (76–80), c1–c2 44 (43–47), d–d 45 (44–47), f–f 22 (20–23). Seta sc2 laterad and slightly posterior to sc1; seta c1 closer to d than to c2, anterolateral to the latter.

Idiosoma – venter (Figs 10–11): setae 1a 6 (5–6) posteriad of apodemes 1; setae 2a 7 (7–8) located in the center of coxisternal plate 2; seta 3a 12 (11–13) located near anterior end of apodeme 3; and seta 3b 12 (10–14) located near middle of apodeme 4. Apodeme 1 fused to anterior end of prosternal apodeme; apodeme 2 not fused to prosternal apodeme. Prosternal apodeme conspicuous between coxisternal plates I but thin between coxisternal plates II, extending close to sejugal apodeme. Sejugal apodeme conspicuous. Lines of fusion between coxae III and IV with venter of idiosoma mostly conspicuous (apodemes 3 and 4, poststernal apodeme and connecting apodeme between apodemes 3 and 4); connecting apodemes between apodemes 4 and poststernal diffuse.

Legs (Fig. 12): lengths (measured from femur to tarsus): leg I 63 (62–65), leg II 59 (57–61), leg III 81 (79–83), leg IV 83 (81–84). Number of the setae (solenidia in parentheses) on femur, genu, tibia and tarsus, respectively: leg I: 4-4-6(2)-9(1), leg II: 3-3-4-4(1), leg III: 1-3-4-3. Claws medium-sized (not reduced) and hooked. Empodia of the legs I, II and III about the same size or slightly smaller compared to the respective basal stalks. Solenidion ω of tarsus I 4 (3–5), stout, wider medially. Sensory cluster of tibia I composed of φ1 3 (3), φ2 4 (4–5) and famulus k 4 (4), all inserted at approximately same level (Fig. 14B). Seta d of tibia I 27 (26–30), serrate. Solenidion ω of tarsus II proximally inserted 4 (4–5) long, stout, wider medially (Fig. 14C). Seta d of tibia II 23 (21–24), serrate. Trochanter IV slightly wider than long, seta v’ 13 (12–14), smooth. Femorogenu IV 41 (40–43) long and 17 (16–19) wide at v’ F level; anterior margin convex, posterior margin slightly convex at proximal third, with a serrate-like projection between these margins. Seta v’ F 9 (8–10), serrate. Setae v’ G 17 (16–18) and l” G 12 (11–13), smooth. Tibia IV 24 (22–26) long; solenidion φ 7 (6–8); seta v’ Ti 28 (27–31), serrate. Tarsus IV short, bearing 3 smooth setae of the following length: tc” 4 (4–5), pv” 6 (5–7) and u’ 5 (4–6). Claw well developed (Fig. 14D).

Type material

Holotype female, allotype male, 6 paratype females and 2 paratype males from Theobroma cacao L., 1 paratype female from Annona muricata L. and 2 paratype females from Spondias purpurea L., 14°47'45"S; 39°10'18"W, Ilhéus, State of Bahia, Brazil, 10/IX/2012, A.C. Lofego and J.M. Rezende. Holotype, allotype, 7 paratype females and 2 paratype males are deposited at DZSJRP and 2 paratype females are deposited at USNM.

Etymology

The species name oliveirai is in honor of Dr. Anibal Ramadan Oliveira (UESC - Universidade Estadual Santa Cruz from Ilhéus-BA) for his contribution to study of mites and for all his support during the samplings in the region.

Figure 1. 

Daidalotarsonemus oliveirai sp. n. (female). Dorsal surface.

Figure 2. 

Daidalotarsonemus oliveirai sp. n. (female). Dorsal micrographs. A phase contrast B differential interference contrast C low temperature scanning electron microscopy.

Figure 3. 

Daidalotarsonemus oliveirai sp. n. (female). Ventral surface.

Figure 4. 

Daidalotarsonemus oliveirai sp. n. (female). Ventral micrographs. A phase contrast B differential interference contrast C low temperature scanning electron microscopy.

Figure 5. 

Daidalotarsonemus oliveirai sp. n. (female). A leg I B leg II C leg III D leg IV.

Figure 6. 

Daidalotarsonemus oliveirai sp. n. (female). Detail of the gnathosoma.

Figure 7. 

Daidalotarsonemus oliveirai sp. n. (female). A sensorial cluster of tibia I B Solenidion ω of tarsus II C Bothridial seta sc1D lateral view of the setae d, e and fE posterior view of the setae d, e and fF detail of the tegula.

Figure 8. 

Daidalotarsonemus oliveirai sp. n. (male). Dorsal surface.

Figure 9. 

Daidalotarsonemus oliveirai sp. n. (male). Dorsal micrographs. A phase contrast B differential interference contrast C low temperature scanning electron microscopy.

Figure 10. 

Daidalotarsonemus oliveirai sp. n. (male). Ventral surface.

Figure 11. 

Daidalotarsonemus oliveirai sp. n. (female). Ventral micrographs. A phase contrast B differential interference contrast C low temperature scanning electron microscopy.

Figure 12. 

Daidalotarsonemus oliveirai sp. n. (male). A leg I B leg II C leg III D leg IV.

Figure 13. 

Daidalotarsonemus oliveirai sp. n. (male). Detail of the gnathosoma.

Figure 14. 

Daidalotarsonemus oliveirai sp. n. (male). A gnatosoma B sensorial cluster of tibia I C tarsus II D part of tibia and tarsus IV.

Excelsotarsonemus caravelis Rezende, Lofego & Ochoa, sp. n.

http://zoobank.org/101417BE-223C-4746-9107-05528AD1A7F8
Figs 15, 16, 17, 18, 19, 20, 21

Diagnosis

Females of this species resemble those of Excelsotarsonemus kimhansenae Ochoa & OConnor because of the shape of dorsal setae v1, sc2, c1 and c2, and the ornamentation pattern on the prodorsum; but they are distinguished by the asymmetric shape of setae e and the U-shaped cerotegument accumulation between prodorsum and tergite C in Excelsotarsonemus caravelis sp. n., whereas setae e are orbicular and smooth and tergite C surface is smoother in E. kimhansenae. The accumulation of the cerotegument between the tergites was easily noticed in all microscopy techniques used (Fig. 16), and it is being considered a taxonomic feature, useful for distinguishing these species.

Adult female

(5 specimens measured). Gnathosoma (Figs 17, 20, 21A-B): completely covered by prodorsum. Subtriangular in ventral view, length 22 (21–24), maximum width 17 (16–19); dorsal apodeme distinct. Setae dgs 7 (7–8) and vgs 5 (5–6) smooth; palps moderately short 6–8 (7), with 2 small subterminal setae and terminal projections. Pharynx fusiform, 15 (15–16) long and 6 (6) wide at maximum width. Gnathosoma, idiosoma and legs covered with tiny dimples, each 0.3 (0.2–0.5) in diameter.

Idiosoma – dorsum (Figs 15–16): length 167 (166–168), width at level of c1 86 (84–90); prodorsal shield normally covering entire gnathosoma, with three external humps, broader proximally, central area with an inverted Y-shaped pattern. Stigma near lateral notch of the prodorsal shield, equidistant to the v1 and sc2 setal bases. Entire dorsum covered with cerotegument with a U-shaped cerotegument accumulating between the prodorsum and tergite C (Fig. 16). Tergite D with irregular bumps near setae d. Lengths of the setae: v1 29 (27–31), sc1 16 (14–18) (Fig. 21C), sc2 47 (45–49), c1 40 (40–41) (Fig. 21E), c2 9 (8–10), d 30 (28–32) (Fig. 21F), e 16 (16–17), f 36 (35–38) and h 13 (11–16). Maximum width of expanded setae: sc2 3 (3–4), c1 11 (11–12), d 22 (21–23), e 32 (31–33) and f 12 (11–13). All setae serrate, except for c2 which is smooth. Bothridial setae sc1 capitate with tiny spines; sc2 linear with a strong central furrow; setae c1 lanceolate, d ovate and f oblanceolate with serrate central veins; e each totally asymmetric (Figs 21G-H). Distances between dorsal setae: v1–v1 26 (24–29), sc2–sc2 46 (45–48), v1–sc2 15 (14–16), c1–c1 43 (41–45), c2–c2 89 (85–96), c1–c2 36 (34–38), d–d 27 (27–28), f–f 11 (9–13), e–f 12 and h–h 5 (4–7). Seta sc2 located anteriorly to sc1. Dorsal cupules not easily seen.

Idiosoma – venter (Figs 17–18): seta 1a 6 (6–7), posteriad of apodemes 1; 2a 9 (9–10), posterolaterad of apodemes 2; 3a 11 near anteriomedial margins of apodemes 3; 3b 8 (8–9) on posterior margins of apodemes 4. Apodeme 1 conspicuous and fused to anterior end of prosternal apodeme. Apodeme 2 short and not fused to prosternal apodeme. Prosternal apodeme conspicuous from junction with apodeme 1 near middle of sejugal apodeme portion. Sejugal apodeme uninterrupted with several small indentations. Apodeme 3 with a constriction near anterior end, extending diagonally from proximity of base of seta 3a to anterior margin of trochanter III; apodeme 4 extending diagonally from the middle of the poststernal apodeme to base of seta 3b. Poststernal apodeme bifurcated anteriorly. Tegula wide 16 (15–17) and very short, 4 (4–5) (Fig. 21I), posterior margin slightly arched. Setae ps 17 (16–19) smooth.

Legs (Fig. 19): lengths (measured from femur to tarsus): leg I 42 (42–43), leg II 40 (39–41), leg III 92 (89–95), leg IV 32 (31–35). Number of setae (solenidia in parentheses) on femur, genu, tibia and tarsus, respectively: leg I: leg I: 3-4-5(2)-7(1), leg II: 3-3-4-4(1), leg III: 2+2-4-4. Claws medium-sized (not reduced) and hooked. Empodia of the legs I, II and III about the same size or slightly smaller compared to the respective basal stalks. Tarsal solenidion ω of tibiotarsus I 4 (4–5), stout, wider medially. Sensory cluster of tibia I complete (Fig. 21D), solenidion φ1 4 (4–5), slender, capitate; solenidion φ2 3, robust, slightly capitate; famulus k 6; all those inserted at approximately in the same level. Seta d of tibia I 23 (22–24), serrate. Solenidion ω of tarsus II proximally inserted, 4 long, stout, wider medially. Seta d of tibia II 17 (17–18), serrate. Femorogenu IV 18 (16–20); tibiotarsus IV 9 (9–10). Length of leg IV setae: v’ F 8 (8–9), v’ G 10 (10–11), v’ Ti 23 (22–24) and tc” 31 (29–33); setae v’ Ti and tc” smooth; v’ Ti falcate.

Adult male

Unknown.

Type material

Holotype female and 4 paratype females on Theobroma cacao L., 14°47'45"S; 39°10'18"W, Ilhéus, State of Bahia, Brazil, 10/IX/2012, A.C. Lofego and J.M. Rezende. Holotype and 3 paratypes are deposited in the DZSJRP and 1 paratype is deposited in the USNM.

Etymology

The region where this mite was found is the same place as the first Portuguese explorers arrived in Brazil, at the end of 15th century. On their trip, they used caravels, which had big sails. The name caravelis is used because several dorsal setae of this mite species are held in the upright position resembling those sails.

Note

Setae f has a unique modification as it is oblanceolate dorsal view, with four faces attached by the main vein, giving a deep concavity at either site, with a central furrow dorsally shoe-like; all margins serrate (Fig. 21H). Similar setal complex modification has been observed in E. mariposa (setae d, f and e) and other Excelsotarsonemus and Daidalotarsonemus species under DIC. However, it is under the LT-SEM that we can understand their complexity.

Figure 15. 

Excelsotarsonemus caravelis sp. n. (female). Dorsal surface.

Figure 16. 

Excelsotarsonemus caravelis sp. n. (female). Dorsal micrographs. A phase contrast B differential interference contrast C low temperature scanning electron microscopy.

Figure 17. 

Excelsotarsonemus caravelis sp. n. (female). Ventral surface.

Figure 18. 

Excelsotarsonemus caravelis sp. n. (female). Ventral micrographs. A phase contrast B differential interference contrast C low temperature scanning electron microscopy.

Figure 19. 

Excelsotarsonemus caravelis sp. n. (female). A leg I B leg II C leg III D leg IV.

Figure 20. 

Excelsotarsonemus caravelis sp. n. (female). Detail of the gnathosoma.

Figure 21. 

Excelsotarsonemus caravelis sp. n. (female). A gnatosoma B detail of the palps C Bothridial seta sc1D sensorial cluster of tibia I E seta c1F seta dG tergites D, E, F, H and posterior setae H setae e, f and hI tegula.

Figure 22. 

Excelsotarsonemus tupi sp. n. (female). Dorsal surface (arrows indicate muscle attachments present over the body).

Excelsotarsonemus tupi Rezende, Lofego & Ochoa, sp. n.

http://zoobank.org/B37CCDE2-2748-47BD-B46B-801AD0F22D6F
Figs 22, 23, 24, 25, 26, 27, 28

Diagnosis

Females of this species resemble those of Excelsotarsonemus kaliszewskii Ochoa & Naskręcki (Ochoa et al. 1995) because of the similar shape of setae sc2, c1 and d. However, setae c2 and e of Excelsotarsonemus tupi sp. n. are setiform-like, while in E. kaliszewskii these setae are falcate and elongate. In addition, the humps on the prodorsum and the muscle attachments of tergite D are very different in shape between these two species, being more ornate and prominent in E. kaliszewskii.

Adult female

(3 specimens measured). Gnathosoma (Figs 24 and 27): completely covered by the prodorsum. Subtriangular in ventral view, length 21 (21–22), maximum width 17 (16–19); dorsal apodeme distinct. Setae dgs 8 (7–9) and vgs 4 (4–5) smooth; Palps moderately short 6–8 (7), with 2 small subterminal setae and terminal projections. Pharynx fusiform, 15 (14–16) long and 8 (7–9) wide at maximum width region. Gnathosoma, idiosoma and legs covered with tiny dimples, each around 0.3 (0.2–0.5) in diameter.

Idiosoma – dorsum (Figs 22–23): length 175 (171–179), width at level of c1 94 (93–95); prodorsal shield covering gnathosoma. Entire dorsum covered with cerotegument. Stigma inserted proximally at the lateral notch of the prodorsal shield, near the base of setae v1. Prodorsum, tergites C and D with distinct muscle attachments, visible with DIC and PC optic microscopes. Lengths of the setae: v1 23 (22–25) (Fig. 28C), sc1 15 (15–16) (Fig. 28B), sc2 44 (43–47) (Fig. 28D), c1 46 (44–49) (Fig. 28E), c2 14 (11–17), d 32 (31–34), e 26 (25–29), f 36 (35–37) and h 19 (19–20). Maximum width of expanded setae: sc2 12 (11–13), c1 8 (8–9), d 22 (21–23), e 3 (3–4) and f 22 (21–23). All dorsal setae serrated. Bothridia sc1 capitate with tiny spines. Setae v1 linear; c2 setiform; c1 oblong very elongated; sc2 lanceolate with three heavy dorsal veins; d ovate and f asymmetrical, both with internal cells; e linear, heavily serrate (Figs 28F-H); h elliptical, serrate with one dorsal vein. Distances between dorsal setae: v1–v1 37 (37–38), sc2–sc2 48 (47–49), v1–sc2 16 (15–18), c1–c1 45 (44–46), c2–c2 76 (74–80), c1–c2 17 (16–19), d–d 25 (23–28), f–f 11 (9–15), e–f 13 (11–16) and h–h 10 (9–14). Seta sc2 located lateral to sc1. Dorsal cupules not easily seen.

Idiosoma – venter (Figs 24–25): setae 1a 5 (4–7), inserted on tubercles posteriad of apodemes 1; 2a 7 (6–10), posterolaterad of apodemes 2; 3a 8 (7–11) near anteriomedial margins of apodemes 3; 3b 6 (5–9) on posterior margins of apodemes 4. Apodeme 1 conspicuous, fused to anterior end of prosternal apodeme. Apodeme 2 short and not fused to prosternal apodeme. Prosternal apodeme not clearly united with sejugal apodeme, continuous along length to level of apodemes 2, ending in a diffuse area that reaches to sejugal apodeme. Sejugal apodeme uninterrupted. Apodeme 3 with a constriction near anterior end, extending diagonally from proximity of base of seta 3a to anterior margin of trochanter III; apodeme 4 extending diagonally from the middle of the poststernal apodeme to base of seta 3b. Poststernal apodeme bifurcated anteriorly. Externally, apodemes 3 and 4 surrounded by a distinct punctation. Tegula wide 16 (15–17) and very short 4 (4–5) with posterior margin slightly arched. Seta ps 6 (15–6) smooth.

Legs (Fig. 26): lengths (measured from femur to tarsus): leg I 44 (43–48), leg II 40 (39–41), leg III 90 (88–93), leg IV 33 (31–35). Number of setae (solenidia in parentheses) on femur, genu, tibia and tarsus, respectively: leg I: 3-4-4(2)-7(1), leg II: 3-3-4-4(1), leg III: 0+3-4-4. Claws medium-sized (not reduced) and hooked. Empodia of the legs I, II and III about the same size or slightly smaller compared to the respective basal stalks. Tarsal solenidion ω of tibiotarsus I 4 (4–5), stout, wider medially. Sensory cluster of tibia I incomplete, solenidion φ1 4, slender, capitate; famulus k 6 (6–7); both inserted at approximately the same level (Fig. 28A). Seta d of tibia I 21 (20–22), serrate. Solenidion ω of tarsus II proximally inserted, 4 long, stout, wider medially. Seta d of tibia II 18 (17–21), serrate. Femorogenu IV 19 (19–20); tibiotarsus IV 8 (7–9). Length of leg IV setae: v’ F 7 (7–8), v’ G 10 (9–11), v´ Ti 18 (19–23) and tc” 25 (23–28); setae v’ Ti and tc” smooth; v’ Ti falcate.

Adult male

Unknown.

Type material

Holotype female and 2 paratype females on Theobroma cacao L., 14°47'45"S; 39°10'18"W, Ilhéus, State of Bahia, Brazil, 10/IX/2012, A. C. Lofego and J.M. Rezende. Holotype and 2 paratype females are deposited in the DZSJRP.

Etymology

The species name tupi is in honor of a Tupi people, one of the most important native indigenous tribes in Brazil which used to live in all coastal region where this mite species was found.

Figure 23. 

Excelsotarsonemus tupi sp. n. (female). Dorsal micrographs. A phase contrast B differential interference contrast C low temperature scanning electron microscopy.

Figure 24. 

Excelsotarsonemus tupi sp. n. (female). Ventral surface.

Figure 25. 

Excelsotarsonemus tupi sp. n. (female). Ventral micrographs. A phase contrast B differential interference contrast C low temperature scanning electron microscopy.

Figure 26. 

Excelsotarsonemus tupi sp. n. (female). A leg I B leg II C leg III D leg IV.

Figure 27. 

Excelsotarsonemus tupi sp. n. (female). Detail of the gnathosoma.

Figure 28. 

Excelsotarsonemus tupi sp. n. (female). A sensorial cluster of tibia I B Bothridial seta sc1 and stigma opening C seta v1D seta sc2E seta c1F lateral view of the setae d, e, f and hG posterior view of the setae d, e, f and hH insertion of seta fI posterior view of tergites E, F and H (which is indicated by an arrow).

Discussion

Some characters of Daidalotarsonemus, Excelsotarsonemus and other tarsonemids in general have been misunderstood or have not been clearly interpreted, certainly because of the reliance on only light microscopy technology. This becomes clear by comparing LT-SEM micrographs with the drawings of species described previously. The use of LT-SEM and other SEM techniques by acarologists is useful to truly understanding morphological details of the mites, and contributing to more accurate and reliable taxonomic and systematic studies.

The extension of the prodorsum over the gnathosoma in the genera Daidalotarsonemus and Excelsotarsonemus is a feature mentioned by Lindquist (1986) and Ochoa et al. (1995), respectively. Using the LT-SEM, it was observed the gnathosoma has the ability to protract and retract, being covered by the prodorsum and the coxisternal plates I (Figs 4, 18 and 25).This is a difficult character to discern using light microscopy, mainly because slide mounting distorts it by the flattening of the specimen between the slide and the coverslip, often pushing the gnathosoma forward. In the Daidalotarsonemus species studied, it was observed these mites are able to partially retract the gnathosoma under the propodosoma, leaving the distal part, including the palps exposed. The two species of Excelsotarsonemus are able to retract the entire gnathosoma, similar to turtles, under the propodosoma and over the apodemes 1.

Both genera studied, especially Excelsotarsonemus, have some dorsal setae (especially sc2, c1, d, e and f) with very broad and intricate folding patterns. It is not clear the function of these setae yet. Each one has strong veins that probably help it raise up and maintain itself perpendicular to the body. These sail-like setae might allow them to become airborne, gliding within the canopies and colonizing new trees (Ochoa and OConnor 1998). Setae e and f, because of their position and the way they lay above tergite H, seem to have different functions, perhaps related to protection, entrapping fungal spores and/or improving the aerodynamic characteristics of the mites. Some setae have even more complicated patterns, e.g. the setae e of Excelsotarsonemus caravelis (clearly asymmetric) and setae f of Excelsotarsonemus tupi (asymmetrical and with internal cells). Furthermore, setae d in both species apparently sits on the modified setae e or f like a lid (Fig. 21G, 21H, 28F, 28H). Tergite EF and its setae are supported by plate H, which is concave; both plates are partially covered by the posterior projection of tergite D (Fig. 28I).

It was noticed the production of cerotegument (Krantz 2009) over the body of both genera. Using LT-SEM, the cerotegument was captured extending over the body with fungi, lichens and bacteria accumulating on it. The cerotegument along with its attached material are shed at the edge of the tergites, especially on the propodosoma and tergites C and D (Figs 2C, 4C, 9C, 16C, 18C, 23C and 25C), indicating a way these mites might disseminate microorganisms and even plant pathogens. Although these mites were preserved in 70% alcohol for about eight months, the cerotegument still contained fungi and bacteria. The primary purpose of this substance appears to be water retention, but it also may allow the mite to cover itself in another layer of particles if the substance is sticky (Walter and Proctor 2013). This fact has important biological and agricultural implications. First, this substance allows them to carry debris over their body when they disperse between the canopies. Also, the cerotegument could protect the mite against harmful fungi, being a barrier between them and the soft cuticle. Lastly, by carrying fungi and bacteria, they may act as reservoirs of microorganisms (including plant pathogens) to their host plants, and spreading them throughout the forests and surrounding crops. More studies on the biology and feeding parameters of these genera are necessary to better understand their role and impact.

The discovery of three new mite species in such a small sampling area is remarkable. Although South America has five of the biodiversity hotspots biomes of the world (Myers et al. 2000), just 10 tarsonemid species have been described based on specimens found in this region (Lofego et al. 2005, Lofego and Gondim Jr. 2006, Lofego and Feres 2006, Lofego et al. 2007, Moraes et al. 2002). In addition, two species of Daidalotarsonemus and three of Excelsotarsonemus were found in very similar rainforest areas in Costa Rica (Ochoa et al. 1991; Ochoa et al. 1995, Ochoa and OConnor 1998). Most of these mite species in Costa Rica and Brazil were collected on cocoa trees. This tropical crop has broad leaves which are often covered with fungi and lichens, making it a perfect collecting trap of falling insects and mites from the surrounding tree canopy. Undoubtedly, there is much more to be learned of the species composition, biology and ecology of tarsonemid species present in this rainforest. It is also alarming to think about how much biological information is probably being lost even before it becomes known to the scientific community due to deforestation. For this reason, it is imperative to conduct more surveys to increase the knowledge of the fauna of Tarsonemidae and other mite families in forest canopies around the world.

Acknowledgements

To FAPESP (Fundação de Amparo a Pesquisa do Estado de São Paulo) (Procs. 2011/19890-0 and 2013/08402-0) for its financial support. To Prof. Dr. Anibal R. Oliveira (UESC) for his support during the samplings in Bahia State. To Nit Malikul, Debra Creel (SEL-USDA) for their technical support and to Chris Pooley (ECMU-USDA) for their help with the LT-SEM images. To Dr. Gregory Evans (APHIS-USDA), for helpful suggestions and careful review of the manuscript. To Dr. Cal Welbourn (DPI-FDACS) and Dr. Evert Lindquist (BRCAC) for their comments and suggestions. To the Smithsonian Natural History Museum and National Agricultural Library (NAL-USDA), SEL-USDA for support and assistance with references for this study. 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.

References

  • Bolton SJ, Klompen H, Bauchan GR, Ochoa R (2014) A new genus and species of Nematalycidae (Acari: Endeostigmata). Journal of Natural History 48(23–24): 1359–1373. doi: 10.1080/00222933.2013.859318
  • Fisher JR, Dowling PG (2010) Modern methods and technology for doing classical taxonomy. Acarologia 50(3): 395–409. doi: 10.1051/acarologia/20101981
  • Krantz GW (2009) Form and Function. In: Krantz GW, Walter DE (Eds) Texas Tech University Press, Lubbock, 5–53.
  • Magowski W, Di Palma A (2000) Acaronemus tamaricis, a new species of the family Tarsonemidae (Acari, Heterostigmata) from France. International Journal of Acarology 26: 127–136. doi: 10.1080/01647950008684177
  • Moraes GJ de, Lindquist EE, Lofego AC (2002) A new genus and species of tarsonemid mite (Acari: Tarsonemidae) associated with a Neotropical curculionid beetle (Coleoptera). Invertebrate Systematics 16: 687–695. doi: 10.1071/IT01030
  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853–858. doi: 10.1038/35002501
  • Lin J, Zhang ZQ (2002) Tarsonemidae of the world: Key to genera, geographical distribution, systematic catalogue & annotated bibliography. Systematic and Applied Acarology Society, London, 440 pp.
  • Lindquist EE (1986) The world genera of Tarsonemidae (Acari: Heterostigmata): a morphological, phylogenetic and systematic revision, with classification of family-group taxa in the Heterostigmata. The Entomological Society of Canada, Ottawa, 517 pp.
  • Lofego AC, Gondim Jr MGC (2006) A new species of Steneotarsonemus (Acari: Tarsonemidae) from Brazil. Systematic and Applied Acarology 11: 195–203.
  • Lofego AC, Feres RJF (2006) A new genus and species of tarsonemid mite (Acari: Tarsonemidae) from Brazil. Zootaxa 1299: 45–55.
  • Lofego AC, Moraes GJ de, Ochoa R (2007) Four new species of Xenotarsonemus (Acari: Tarsonemidae) from Brazil. Zootaxa 1646: 1–15.
  • Lofego AC, Ochoa R, Moraes GJ de (2005) Some tarsonemid mites (Acari: Tarsonemidae) from the Brazilian “Cerrado” vegetation, with descriptions of three new species. Zootaxa 823: 1–27.
  • Ochoa R, Naskrecki P, Colwell RK (1995) Excelsotarsonemus kaliszewskii, a new genus and new species from Costa Rica (Acari: Tarsonemidae). International Journal of Acarology 21(2): 67–74. doi: 10.1080/01647959508684045
  • Ochoa R, OConnor BM (1998) Two new species of the genus Excelsotarsonemus (Acari: Tarsonemidae). International Journal of Acarology 24(3): 179–187. doi: 10.1080/01647959808683583
  • Ochoa R, Smiley RL, Saunders JL (1991) The family Tarsonemidae in Costa Rica (Acari: Heterostigmata). International Journal of Acarology 17(1): 41–86. doi: 10.1080/01647959108683885
  • Smiley RL (1967) Further studies on the Tarsonemidae. Proceedings of the Entomological Society of Washington 69(1): 127–146.
  • Smiley RL (1969) Further studies on the Tarsonemidae, II. Proceedings of the Entomological Society of Washington 71(2): 218–229.
  • Sousa JM, Lofego AC, Gondim Jr MGC (2014) Two new species of tarsonemid mites (Acari: Tarsonemidae) from northeastern Brazil. Zootaxa 3889(3): 429–441. doi: 10.11646/zootaxa.3889.3.5
  • Walter DE, Proctor HC (2013) Mites: Ecology, Evolution & Behaviour. Springer, New York, 494 pp. doi: 10.1007/978-94-007-7164-2
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