Three new species of Eurypon Gray, 1867 from Northeastern Brazil (Poecilosclerida; Demospongiae; Porifera)

Zootaxa 3895 (2): 273–284 www.mapress.com /zootaxa / Copyright © 2014 Magnolia Press

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http://dx.doi.org/10.11646/zootaxa.3895.2.8 http://zoobank.org/urn:lsid:zoobank.org:pub:12702F5B-4E55-4CCA-8664-1F6269EF06EA

Three new species of Eurypon Gray, 1867 from Northeastern Brazil (Poecilosclerida; Demospongiae; Porifera) GEORGE GARCIA SANTOS, FERNANDO FRANÇA & ULISSES PINHEIRO1 Universidade Federal de Pernambuco, Centro de Ciências Biológicas, Departamento de Zoologia, Av. Nelson Chaves, s/n Cidade Universitária CEP 50373-970, Recife, PE, Brazil. 1 Corresponding author. E-mail: [email protected]

Abstract Three new species of Eurypon from Northeastern Brazil are described: Eurypon clavilectuarium sp. nov.; Eurypon suassunai sp. nov. and Eurypon distyli sp. nov. Samples were collected from the continental shelf of Rio Grande do Norte, Bahia and Paraíba States. While the majority of Atlantic Eurypon species have been described from deep water, two of three new species described in this study were collected from shallow depths. The three new species from Brazil were compared with all other eighteen Eurypon species described from the Atlantic. Key words: Porifera, sponge, Eurypon, new species, Rio Grande do Norte State, Paraíba State, Bahia State, taxonomy, Brazil

Introduction Eurypon Gray, 1867 is essentially an encrusting sponge with hymedesmioid or microcionid skeletal arrangement (Hooper 2002), the difference between the two being related to the relative thickness of species. The most recent revision of the genus (Aguilar-Camacho & Carballo 2013) describes four new species from the Mexican Pacific Ocean, essentially summarized as follows. The morphology of echinating acanthostyles of Eurypon is similar to that found in species belonging to the subgenus Microciona (Genus Clathria; Family Microcionidae). The hymedesmioid skeleton of Eurypon is a homoplasious character that had been reported in several other genera (such as: Clathria, Acarnus, Hymedesmia, Timea, Prosuberites and others) (Boury-Esnault et al. 1994; Hooper 1996). Species of Eurypon have tylostyles (or subtylostyles) in one or two categories and acanthostyles as choanosomal spicules (both of which echinate and are erect on the hymedesmoid basal spongin skeleton), and one or more categories of oxeas or styles as subectosomal or ectosomal spicules (the former associated with the erect tylostyles and the latter tangential or forming brushes on the surface). Microscleres if present are raphides (Hooper 2002; Aguilar-Camacho & Carballo 2013). Topsent’s (1894) description mentions dubious chelae and asters (in E. toureti), but these are indeed foreign as he suspected (Hooper 2002). The genus currently has 45 valid species with 20 recorded in the Atlantic Ocean, and five of these also occurring in the Mediterranean Sea (Bertolino et al. 2013; van Soest et al. 2014). So far in Brazil the only records of the genus are from Amapá State (Collette & Rützler 1977) and Pernambuco State (Muricy & Moraes 1998), neither of which identified specimens to a species taxon. In this study, three new species of Eurypon are described from Northeastern Brazil, increasing to 23 the number of known species in the Atlantic.

Material and methods Specimens of Eurypon were collected from four localities in Northeastern Brazil (Figure 1). One specimen was

Accepted by J. Hooper: 13 Nov. 2014; published: 15 Dec. 2014

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collected from one trawl at Rio Grande do Norte State on 2011, as part of the Project ‘Campanha de Monitoramento Ambiental do Projeto de Caracterização Ambiental do Talude Continental na Bacia Potiguar/ Rio Grande do Norte/ BR’ (BPot) sponsored by PETROBRAS (Petróleo do Brasil S/A). Other specimens from Paraíba and Bahia States were collected by snorkeling. Specimens were preserved in 80% ethanol and deposited in the Porifera collection of Universidade Federal de Pernambuco (UFPEPOR). Dissociated spicule mounts and skeletal sections were made using classical procedures for Demospongiae (Hajdu et al. 2011). Images of specimens, sections and SEM (Scanning Electron Microscopy) preparations were obtained digitally. Spicule measurements from each specimen are presented as minimum–mean–maximum for length/width, with n = 30. Taxonomic comparisons were made with data tabulated for all species of Eurypon available in the World Porifera Database (van Soest et al. 2014).

FIGURE 1. Location of the collection sites of Eurypon clavilectuarium sp. nov. (1—Rio Grande do Norte State); Eurypon distyli sp. nov. (2—Paraíba State); and Eurypon suassunai sp. nov. (3, 4—Bahia State).

Results and discussion Systematics Class Demospongiae Order Poecilosclerida Topsent, 1928 Remarks. From recent molecular evidence it has been proposed to resurrect the concept of Axinellida, although different in composition from that proposed by Levi (1973) (see Morrow et al. 2012). For the present, until more fully resolved through better taxón sampling for new molecular evidence, we follow the current systematics usage of the World Porifera Database (van Soest et al. 2014).

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Family Raspailiidae Nardo, 1833 Subfamily Raspailiiniae Nardo, 1833 Genus Eurypon Gray, 1867 Synonymy. For synonymy see Hooper (2002). Definition. Typically encrusting Raspailiidae with microcionid skeletal structure in which fibre nodes ascend from the basal layer of spongin (Hooper 2002). Type species: Hymeraphia clavata Bowerbank, 1866 (by monotypy).

Eurypon clavilectuarium sp. nov. (Figs 1–3; Table 1) Type specimens: UFPEPOR 1534 (Holotype), Bacia Potiguar (04º 44.8945' S, 36º 25.4571' W), Rio Grande do Norte State, Brazil, depth 108 m, trawl, Box 37, col. Petrobras, (23.V.2011). Diagnosis. Eurypon clavilectuarium sp. nov. is the only Eurypon described from the Atlantic with large choanosomal subtylostyles (1200–2000 µm long), and raphidiform styles (440 µm long). External morphology (Fig. 2A–B). Encrusting sponge (in calcareous nodules), up to 1 mm thick. Oscules not visible. Surface hispid due to evenly distributed projecting spicules. Consistency is fragile. Color in life is unknown and brownish-purple in ethanol. However, the specimens were collected in the same drag as Aiolochroia crassa (Hyatt, 1875) and stored in the same container. It is possible that the A. crassa pigments stained the Eurypon specimens (as also reported for a specimen of Aulospongus by Cavalcanti et al. 2014). Skeleton (Fig. 2C). Skeletal structure is hymedesmioid composed by long subtylostyles, two categories of echinating acanthostyles and raphidiform styles with their bases embedded in basal spongin and points protruding a long way through the surface, forming a dense erect palisade on the basal spongin.

FIGURE 2. Eurypon clavilectuarium sp. nov. (UFPEPOR 1534, holotype). A, preserved specimen; B, details of the surface; C, skeleton. Scale bars: A = 1 cm; B = 1.5 mm; C = 250 µm.

Spicules (Fig. 3A–G). Choanosomal subtylostyles (Fig. 3A, E): long, smooth, slender, slightly curved and with bulbous to styloid base (1200–2000 / 8–24 µm); Acanthostyles I (Fig. 3B, F): varying from straight to slightly curved, with lightly bulbous base, short and curved spines (hook-shaped spines) more concentrated in the

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middle and apical part of spicules. Spination along the shaft is very sparse (195–600 / 7–17 µm). Acanthostyles II (Fig. 3C, G): straight, fusiform, base frequently styloid, totally microspined (spines are always recurved and arranged the same as previous category) (72–114 µm); Raphidiform styles (Fig. 3D): long, smooth, with styloid base, slender, ranging from straight to curved, some sinuous (260–439 / 1.9–3 µm).

FIGURE 3. Spicule composition of Eurypon clavilectuarium sp. nov. (UFPEPOR 1534, holotype) in SEM. A, subtylostyle; B, acanthostyle I; C, acanthostyle II; D, raphidiform style; E, details of ends of A; F, details of ends of B; G, details of ends of C. Scale bars: A = 150 µm; B = 60 µm; C–D = 30 µm; E–G = 10 µm.

Distribution (Fig. 1). Northeastern coast of Brazil, Rio Grande do Norte State, Brazil. Depth. 108 m. Etymology. The species is named clavilectuarium (clavus = nail, lectuarius = of a bed), due to the long spicules perpendicular and projecting from the basal spongin on the substate, resembling a bed of nails. Remarks. The new species belongs to the genus by the presence of choanosomal subtylostyles, echinating acanthostyles, subectosomal raphidiform styles, and an encrusting habit. Eurypon clavilectuarium sp. nov. is the unique species of the genus from Atlantic which has large choanosomal subtylostyles (1200–2000 µm) and raphidiform styles (439 µm). The presence of two categories of acanthostyles in E. clavilectuarium sp. nov. differs the following species from Atlantic: E. cinctum Sarà, 1960; E. clavatella Little, 1963; E. coronula (Bowerbank, 1874); E. fulvum Lévi, 1969; E. lacazei (Topsent, 1891); E. lictor (Topsent, 1904); E. major Sarà & Siribelli, 1960;

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E. obtusum Vacelet, 1969; E. radiatum (Bowerbank, 1866); E. toureti (Topsent, 1894); E. viride (Topsent, 1889). Except for E. radiatum, all of these species present tylostyles which are not found in E. clavilectuarium sp. nov. In addition, the following species differ by the presence of oxeas (E. denisae; E. cinctum; E. fulvum; E. major; E. obtusum); tornotes (E. lacazei; E. lictor; E. mucronale); isochelae (E. toureti); and raphides (E. viride) (see character list in Table 1).

Eurypon suassunai sp. nov. (Figs 1, 4–5; Table 1) Type specimens: UFPEPOR 1532 (Holotype), off Canavieiras City, Camamu-Almada Basin (15° 35' 5.91" S, 38° 46' 36.35" W), Bahia State, Brazil, (X.2011). UFPEPOR 1533 (paratype), off Canavieiras City, Camamu-Almada Basin (15° 33' 30.56" S, 38° 45' 14.53" W), Bahia State, Brazil, (X.2011). Diagnosis. Eurypon suassunai sp. nov. is the only Eurypon from the Atlantic which combines subtylostyles, acanthostyles I, acanthostyles II with bulbous base, and raphidiform styles. External morphology (Fig 4A–B). Thin transparent encrustation, about 1 mm thick. Oscules not visible. Surface hispid due to evenly distributed projecting spicules. Consistency is fragile. Color in life is orange (formaldehyde) and pale in ethanol. Skeleton (Fig. 4C–D). Ectosomal skeleton is absent. Tips of the choanosomal spicules protrude externally (Fig. 4C–D). The choanosomal skeleton has a hymedesmioid structure. The raphidiform styles are dispersed in the subectosomal region. Acanthostyles I and II are most abundant on basal layer of spongin (Fig. 2D).

FIGURE 4. Eurypon suassunai sp. nov. (UFPEPOR 1532, holotype). A, arrows indicate the position of the specimen; B, preserved specimen and details of the surface; C, skeleton; D, details of the choanosomal skeleton (hymedesmioid). Scale bars: A = 5 mm; B = 1.5 mm; C = 200 µm; D = 100 µm.

Spicules (Fig. 5A–I). Choanosomal subtylostyles (Fig. 5A, G): long, smooth, slender, slightly curved and with bulbous base (690–1660 / 5–17 µm); Acanthostyles I (Fig. 5B, E): varying from straight to slightly curved, with lightly bulbous base, short and curved spines (hook-shaped spines) more concentrated in the middle and apical part of spicules (159–354 / 7–13 µm); Acanthostyles II (Fig. 5C, F): are short and robust, often straight, with bulbous base, totally microspined with short and curved spines (hook-shaped spines) (54–129 µm); Raphidiform styles (Fig. 5D, H, I): smooth, thin, most are straight, the styloid base ranges from the shape of a crown (171–345 / 1–5 µm). Distribution (Fig. 1). Northeastern coast of Brazil, Bahia State, Brazil. Depth. Shallow water. Etymology. This species is named in honor of the Late the famous writer Ariano Vilar Suassuna for his defense of the culture of the Brazilian Northeast. NEW EURYPON FROM BRAZIL

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Shetlands, Roscoff, Iles de Glénan and Azores Shetland Islands and Norway Vema Seamount

E. clavatum (Bowerbank, 1866) (12)

Azores

Roscoff

E. hispidulum (Topsent, 1904) (3)

E. lacazei (Topsent, 1891) (4)

E. fulvum Lévi, 1969 (2)

E. coronula (Bowerbank, 1874) (10)

Naples Gulf of Mexico

Mediterranean Sea

E. denisae Vacelet, 1969 (10)

E. clavatella Little, 1963 (1)

Paraíba State, Brazil

Eurypon distyli sp. nov.

E. cinctum Sarà, 1960 (10)

Bahia State, Brazil

Rio Grande do Norte State, Brazil

Specimen location

Eurypon suassunai sp. nov.

Eurypon clavilectuarium sp. nov.

Species

40–600

599–880

30–180

60

40–1300

10

70

300–350

1

Shallow water

108

Depth (m)

I) 500 / 17 II) 160–200 / 10– 12 75–80 / 10

75–85 / 9

254

75–102–145 / 5– 6–9 65–600

31–316 / 7–16

I) 120–150 / 7–10 II) 50–90 / 7–8

I) 159–243–354 / 7–10–13 II) 54–77–129 67–89.8–129 / 6–7.1–8

I) 195–329–600 / 7–10–17 II) 72–87–114

Acanthostyles

-

-

-

-

500 / 3

351–361–392 / 4

-

I) 315–398.8–485 / 5–6.9–7 II) 315– 371.3– 437 / 3– 4.3– 4.5 (or anisoxeas) -

171–266–345 / 1– 5 (raphidiform)

Subectosomal Styles 260–354.5–439 / 1.9–2.7–3.1 (raphidiform)

2000 / 20

1100–1500 / 12 -

635–1411

249–384–470 / 14–15–21 1500 / 18

2500 / 8–30

3150 / 29

-

-

Choanosomal Tylostyles -

-

325–365 / 4 (microspined)

-

-

-

-

-

230 / 7 (tornote)

-

475–530 / 7–8 (oxea)

-

-

-

415–510 / 5–9 (style/oxea)

250–300 / 4.5–7.5 (oxea)

122–283.9–373 (raphide)

-

-

Other spicules

......continued on the next page

1060–1701.6–2810 / 7–10.7–18

690–1147–1660 / 5–11–17

Choanosomal Subtylostyles 1200–1659–2000 / 8–17–24

Spicules (µm)

TABLE 1. Comparative micrometric data on the spicules and overview of distribution of the living species of Eurypon Gray, 1867 for the Atlantic. Values are in micrometers (µm), expressed as minimum–maximum or minimum–mean–maximum length/width. References are numbered in parentheses and listed at the foot of the table.

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Gulf of Mexico, Mediterranean and Azores

E. viride (Topsent, 1889) (9) 80–800

Not recorded

900

60–260

650–919

Not recorded

550–1360

250

2460

14–40

650–2165

1600

Depth (m)

85

50–60

I) 1000 / 24 II) 80–300 / 6–13 I) 218 / 8 II) 105 -

I) 2000–3000 / 25–30 II) 170–300 / 15– 25 100–400

I) 700–900 / 25– 30 II) 125–280 / 20 70–170 / 5–7.5

I) 1000 II) 100–320 80–220 / 4–10.5

-

Acanthostyles

-

-

1200 / 8

-

I) 800 / 10–15 II) 350 -

-

-

-

-

-

Subectosomal Styles -

1000

Not recorded

1600 / 14

-

-

-

Not recorded / 10–12 -

1115–2210 / 10–17 -

Not recorded

Choanosomal Tylostyles 2000 / 23

Spicules (µm)

-

-

-

2116 / 27

470–630 /3–4

-

300–480 / 5–6 (microspined)

-

Not recorded

-

Not recorded

Choanosomal Subtylostyles -

70 (raphide)

10–12 (isochelae)

60 (trichodragmata)

-

-

-

-

400–430 / 2.5–3 (oxea)

400–490 / 12–17 (tornote)

480–700 / 4–7.5 (oxea)

575–1000 / 4–5 (tornote) 50 / 13–15 (trichodragmata) -

Other spicules

References: (1) Little (1963); (2) Lévi (1969); (3) Topsent (1904); (4) Topsent (1891); (5) Topsent (1928); (6) Topsent (1927); (7) Bowerbank (1874); (8) Topsent (1894); (9) Topsent (1889); (10) Aguilar-Camacho & Carballo (2013); (11) Bowerbank (1866); (12) Arndt (1935); (13) Burton (1954).

E. toureti (Topsent, 1894) (8)

E. topsenti (Burton, 1954) (13)

Roscoff and Faroes Western Caribbean Gulf of Mexico

Azores, Shetlands and Hebrides Azores

E. simplex (Bowerbank, 1874) (7)

E. scabiosum (Topsent, 1927) (6)

E. radiatum (Bowerbank, 1866) (11)

E. pilosella (Topsent, 1904) (3)

E. obtusum Vacelet, 1969 (10)

E. mucronale (Topsent, 1928) (5)

Mediterranean Sea Azores

Ceuta, Spanish Morocco Naples and Western Europe Azores

E. mixtum (Topsent, 1928) (5)

E. major Sarà & Siribelli, 1960 (10)

Azores

Specimen location

E. lictor (Topsent, 1904) (3)

Species

TABLE 1. (continued)

FIGURE 5. Spicule composition of Eurypon suassunai sp. nov. (UFPEPOR 1532, holotype) in SEM. A, subtylostyle; B, acanthostyle I; C, acanthostyle II; D, raphidiform style; E, details of ends of B; F, details of ends of C; G, details of the base of A; H and I, details of the base of D. Scale bars: A = 200 µm; B = 80 µm; C = 30 µm; D = 80 µm; E–F = 5 µm; G = 10 µm; H–I = 10 µm.

Remarks. Eurypon suassunai sp. nov. belongs to the genus in having choanosomal subtylostyles, echinating acanthostyles and an encrusting habit with a hymedesmioid skeleton. The closest species to E. suassunai sp. nov. is E. clavilectuarium sp. nov. because both shares the same spicules. However, in E. clavilectuarium sp. nov. the subtylostyles are longer and stouter (1200–2000 / 8–24) than those of E. suassunai sp. nov. (690–1600 / 5–17) and in the former, the tyle of the acanthostyles II are styloid against bulbose tyle of the last. Except from both, no others species of Eurypon in Atlantic have raphidiform styles. Furthermore, the presence of two categories of acanthostyles distinguishes E. suassunai sp. nov. from eleven species of the Atlantic: E. cinctum; E. clavatella; E. coronula; E. fulvum; E. lacazei; E. lictor; E. major; E. obtusum; E. radiatum; E. toureti; E. viride (Table 1).

Eurypon distyli sp. nov. (Figs 1, 6–7; Table 1) Type specimens. UFPEPOR 1601 (Holotype), Ponta do Seixas (07º 09' 16" S, 34º 47' 35" W), João Pessoa, Paraíba State, Brazil, depth 1 m, col. G.G. Santos, (05.XI.2013). Paratype. UFPBPOR 1620 (collected together with the holotype).

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Diagnosis. Eurypon distyli sp. nov. is the only Eurypon in the Atlantic with two categories of styles and large raphides. External morphology (Fig. 6). Encrusting sponge, covering surfaces up to 2 cm² diameter and 0.5–1.5 mm thick, growing over rocks (Fig. 6A). Oscules not visible. Surface hispid due to evenly distributed projecting spicules and with some bouquets of spicules irregularly distributed (Fig. 6B). Consistency firm and difficult to tear. Color in life is green, dark green in ethanol.

FIGURE 6. Eurypon distyli sp. nov. (UFPEPOR 1601, holotype). A, fresh holotype taken out of the water, showing spicules; B, details of the surface; C, basal layer of spongin with echinating acanthostyles. Scale bars: A = 1 cm; B = 200 µm; C = 100 µm.

Skeleton (Fig. 6). The ectosomal skeleton is absent, with tips of choanosomal the spicules externally protruding (Fig. 6B). The choanosomal skeleton is a hymedesmioid structure with a basal layer of acanthostyles, auxiliary styles and principal subtylostyles, are all perpendicular to the substrate (Fig. 6B and C). The subectosomal styles I and II are dispersed in the subectosomal region of the erect spicule skeleton. Spicules (Fig. 7A–I). Choanosomal subtylostyles (Fig. 7A, G): long, smooth, slender, slightly curved and with bulbous base (1060–2810 / 7–18 µm); Subectosomal styles I (Fig. 7B, H): smooth, lightly robust and often straight (315–485 / 5–7 µm); Subectosomal style II (anisoxea) (Fig. 7C, I): smooth, thin and varying from straight to curved (315–437 / 3–4.5 µm); Raphides (Fig. 7D): usually straight, smooth and with sharp ends (121–372 / less than 0.5 µm); Acanthostyles (Fig. 7E–F): usually straight, fusiform, with base slightly bulbous and surface completely spined. The spines are short and curved (67–129 µm long), at the base the spines are hookshaped and in the middle region the spines are spatulate (see Fig. 7F). Distribution (Fig. 1). Northeastern coast of Brazil, Paraíba State, Brazil. Depth. 1 m. Etymology. The name refers to the two size categories of subectosomal styles. Remarks. The closest species to Eurypon distyli sp. nov. is E. radiatum from the Azores because both share the posession of two categories of subectosomal styles and one category of acanthostyle, although E. radiatum lacks choanosomal subtylostyles and raphides. Aside from these two species no other Eurypon described from the Atlantic have two categories of subectosomal styles. Other species from Atlantic that resemble Eurypon distyli sp. nov. is E. viride, both having raphides. However, E. viride has small raphides (70 µm long), tylostyles and a white color compared to large raphides (280 µm long), subtylostyles and a green color in E. distyli sp. nov. (Table 1).

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FIGURE 7. Spicule composition of Eurypon distyli sp. nov. (UFPEPOR 1601, holotype). A, subtylostyle; B, style I; C, style II; D, raphide; E, acanthostyle; F, details of the flattened spines; G, details of the base of A; H, details of the base of B; I, details of the base of C. Scale bars: A = 200 µm; B = 40 µm; C = 50 µm; D = 30 µm; E, G, H = 10 µm; F = 5 µm; I = 3 µm.

Discussion The three new species described here display the typical morphology of Eurypon: the presence of choanosomal styles or (sub-)tylostyles, echinating acanthostyles, subectosomal or ectosomal spicules (styles, oxeas and raphides), and an encrusting habit with a hymedesmioid or microcionid basal spongin skeleton (Hooper 2002), the latter depending on how thick the specimens are. We compare the three new species with congeners from the Atlantic, and conclude that they are sufficiently different from our three new species, and therefore are not considered further here. In Raspailiidae, Eurypon is distinguished from Raspailia Nardo, 1833 in having only up to three categories of megascleres whereas typical Raspailia have four categories (Hooper 1991, 2002). According Hooper (2002) this is an attempt to separate species based on their skeletal architecture.

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Many Eurypon species from the Atlantic have so far been described from deep water (40–2165 m), and Picton (1990) proposed this genus was indicative of deep water sponge communities. Although, exceptions have been recorded. Little (1963) described E. clavatella from Gulf of Mexico from 10 m depth, and Sarà & Siribelli (1960) recorded E. major from Western Europe from 14–40 m (van Soest et al. 2000), as well as two species described here from shallow water habitats. With the description of Eurypon clavilectuarium sp. nov., Eurypon suassunai sp. nov. and Eurypon distyli sp. nov., there are now 23 species of the genus in the Atlantic Ocean, and 48 valid species worldwide.

Acknowledgements The authors are grateful to PETROBRAS for donating the holotype (UFPEPOR 1534) specimen and providing collection data. George G.S. thanks CAPES for providing a doctoral scholarship. Authors are also thankful to Mauricio Paiva, Janaina Melo, Dyego Oliveira, Gaby Vasconcelos and Josineide Correia for SEM facilities at CETENE (Centro de Tecnologias Estratégicas do Nordeste), Dr. André Esteves (UFPE), Dr. Jesser Fidelis (UFPE), Dr. Carlos Pérez (UFPE), Thaynã Cavalcante, M.Sc. Lucas Lima (UESPI), Rudá Lucena, Diego Aquino, M.Sc. Luíz Aquino, Yuri Niella, and Adélia Alliz for technical support. We further thank CNPq (Edital PROTAX 2010 562320/2010-5), and FACEPE, for providing grants and/or fellowships, and to two anonymous reviewers for improving the manuscript.

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