Family Smittinidae Levinsen, 1909.

Type genus. Smittina Norman, 1903 (type species Lepralia landsborovii Johnston, 1847, by original designation).

Remarks. Characteristics of the primary orifice, presence of lyrula, avicularium, and presence of pseudopores on the frontal wall and ectooecium, serve as the main taxonomic criteria to distinguishing Smittinidae genera [2, 5, 9, 24, 32]. While most genera encompass fewer than ten species, Parasmittina, Smittina, and Smittoidea are considered highly diverse, with Parasmittina and Smittina comprising more than 100 known species each [1]. Parasmittina and Smittoidea share morphological similarities, leading to misinterpretations regarding diagnostic features and the generic placement of several taxa [4, 18, 19, 20, 21]. Therefore, a taxonomic review of both Parasmittina and Smittoidea is strongly recommended [4, 9, 17].

Type species.

Lepralia jeffreysi Norman, 1876, by original designation.

Diagnosis.

Autozooids with imperforate frontal wall, except for marginal pores. Primary orifice with smooth or beaded distal margin, oral spines usually present, lyrula of variable size and condyles with distinct profiles. Secondary orifice with variable development, sometimes with a proximal pseudosinus. Adventitious avicularia formed from a marginal pore [for example, as in P. jeffreysi (acc. Winston & Hayward [33]), P. nitida and P. winstonae], or sometimes, from a latero-oral pore (for example, as in P. pinctatae, P. simpulata and P. falciformis sp. nov.); adventitious avicularia with diverse shapes and positions (frontal, latero-oral or marginal), but never suboral, unless if displaced by the secondary calcification. Vicarious avicularia may also be present. Ovicells hyperstomial, initially prominent and becoming immersed with secondary calcification; ectooecium with pseudopores (modified from Osburn [24]).

Remarks.

Historically, the taxonomic identification of Parasmittina was primarily based on the morphology and position of the adventitious avicularia [3, 7, 23, 24, 34–37]. Soule & Soule [2, 5] made extensive taxonomic studies on smitinids, particularly Parasmittina, revealing that a combination of morphological characters is necessary for confident identification. However, new species of Parasmittina have been distinguished from congeners primarily based on avicularia morphology (e.g., [7, 10]) or were described based on colonies fragments (i.e., [11, 12, 38]) that may not encompass intraspecific variations of these taxa, especially regarding avicularia development [2, 4, 5, 9, 17, 21, 39].

Thus, in this study, we attempt to analyze colonies at various astogenetic stages, comparing them with all congeners reported worldwide and using both morphological and morphometric data. Diagnostic features were based mainly on the primary orifice (distal margin ornamentation, number of spines, lyrula width, and condyles morphology), avicularia (if adventitious and/or interzooidal, placement, orientation, size, and morphologies), and ooecia (number of pseudopores, and secondary calcification).

Parasmittina abrolhosensis Ramalho, Taylor, & Moraes in Ramalho et al., 2018.

(Figs 1, 2; Tables 1, 10)

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Fig 1. Parasmittina abrolhosensis Ramalho, Taylor, & Moraes in Ramalho et al., 2018.

(A, C–D) UFBA 5004, (B) UFBA 2416, (E) UFBA 696, (F) UFBA 5008, Bahia, Brazil. Arrows indicating avicularia. (A) growing edge of the colony with small avicularia, (B) detail of primary orifice and small elongate avicularia, (C) autozooids with secondary calcification and small avicularia, (D) group of ovicelled zooids with small avicularia, (E) old autozooids with large spatulate avicularia, (F) ovicelled zooids with secondary calcification and large spatulate avicularia. Scale bars: A, C–F = 400 μm; B = 100 μm.

https://doi.org/10.1371/journal.pone.0304347.g001

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Fig 2. Parasmittina abrolhosensis Ramalho, Taylor, & Moraes in Ramalho et al., 2018.

(A–D) USNM 8558, (E–F) USNM 8559, Bahia, Brazil. (A) group of autozooids, (B) detail of an autozooid showing small elongate and subtriangular and large spatulate avicularia, (C) detail of primary orifice, (D) detail of vicarious avicularia, (E) group of young autozooids with small and large avicularia, (F) group of ovicelled zooids. Scale bars: A, E = 500 μm; B, D, F = 200 μm; C = 50 μm.

https://doi.org/10.1371/journal.pone.0304347.g002

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Table 1. Morphometric data of P. abrolhosensis.

Values given in millimeters and represented as minimum–median–maximum (number of zooidal measures). Avicularia abbreviations: Av1 = small elongate; Av2 = small subtriangular bulbous; Av3 = small subtriangular; Av4 = large spatulate; Av5 = vicarious spatulate.

https://doi.org/10.1371/journal.pone.0304347.t001

Smittina areolata: Canu & Bassler 1928: 30, plate 6 Fig 4 [40]. Non Smittina areolata Canu & Bassler, 1927: 23 [41].

Smittina trispinosa spathulata: Canu & Bassler 1928: 29, plate 6, Fig 3 [40]; Parasmittina spathulata: Vieira et al. 2008: 27 (in part) [25], Almeida et al. 2015: 4 (in part) [26]. Non Escharella jacotini var. spathulata Smitt, 1873: 60 [42].

Material examined.

UFPE 813–815; UFBA 2414–2416, 2855–2859, 2861–2862, 2879–2880, 2882–2884, 2886–2888, 3128, 5004–5007, Recife dos Cascos, Baia de Todos os Santos, Bahia, Brazil, 13–21 m, coll. 2016–2017; UFBA 696, 3120, Costa do Dendê, Bahia, Brazil, coll. 2002; UFBA 5008, Camaçari, Bahia, Brazil, 50 m, coll. 07/2004; UFPE 652–661, 2788–2797, Bacia Potiguar, Rio Grande do Norte, coll. 2009–2010; USNM 8558, 8559, Smittina trispinosa spathulata and Smittina areolata, respectively, F. Canu & R. Bassler det., Bahia, Brazil, 49 m, coll. 1876.

Description.

Colony encrusting. Autozooids (Fig 1A) polygonal, almost rhombic, limited by slightly raised lateral walls, surrounded by a single row of 19–23 marginal pores (0.009–0.025–0.042 mm in diameter; n = 30; SD = 0.008 mm). Frontal wall initially smooth in very young zooids (Fig 1A, top; 1B), becoming rough, rugose, and with nodular calcification in older zooids (Fig 1C and 1D). Primary orifice (Fig 1B) elliptical, distal margin smooth, with 1–3 oral spines, lyrula narrow (0.012–0.021–0025 mm wide; n = 30; SD = 0.004 mm); a pair of robust and down-curved hooked condyles with serrated margins. Secondary orifice (Fig 1B and 1C) pear-shaped, forming 2–4 lateral flaps in autozooids, often with in a shallow U-shaped pseudosinus, more pronounced in older or ovicelled zooids (Fig 1D and 1E). Adventitious avicularia variable in shapes and sizes (Fig 1A and 1D), with four morphologies: (1) small, narrow and elongate avicularia (Figs 1C and 1E, 2B and 2E) present at one or both side of the orifice, unequal in size if paired, placed below to the secondary orifice, proximally oriented, rostrum narrow and slightly curved, smooth to slightly corrugated at its lateral margins, rounded tip, palate occupying about half of the rostrum length and oblong foramen; (2) small, subtriangular, bulbous avicularia (Fig 1A and 1D), placed laterally at one side of the orifice, proximally oriented, rostrum subtriangular, pointed tip, palate narrow, reaching twice its initial size with colonial development, leaving a sublanceolate profile; (3) small, narrow and subtriangular to elliptic avicularia (Figs 1C and 1E, 1F, 2B and 2E), placed in zooidal margins and/or in the frontal wall, with smooth lateral margins, rounded tip, palate narrow and elliptical foramen; (4) large spatulate avicularia, more common in older zooids, placed proximolaterally below the orifice, oriented proximally, with rounded distal edge, palate broad, foramen subtriangular, elongate rostrum, with smooth margins and crossbar complete, with 3–4 pseudopores adjacent to the avicularia. (Figs 1F and 2A, 2E); vicarious avicularia (Fig 2D) with the same morphology as the large spatulate avicularia occasionally present. Ovicells (Figs 1D and 2E) globose, initially prominent (Fig 1D) and densely surrounded by adjacent frontal wall in older colonies (Figs 1F and 2F); ectooecium with 18–25 small pseudopores (0.003–0.005–0.008 mm in diameter; n = 30; SD = 0.001 mm), mainly placed at the distal region of the ectooecium surface.

Remarks.

Canu & Bassler [40] studied specimens from northeastern Brazil (Bahia) and attributed them to two species, P. areolata (Canu & Bassler, 1927) [41] and P. spathulata (Smitt, 1873). Following Canu & Bassler [40], Vieira et al. [25] and Almeida et al. [26] attributed other Brazilian specimens to P. spathulata (Smitt, 1873). These P. areolata and P. spatulhata records, as well as new studied specimens from the same region, are here attributed to P. abrolhosensis.

Parasmittina areolata was originally described by Canu & Bassler [41] based on specimens from Hawaii, Pacific Ocean. However, it has been reported in Brazilian coast and in the Caribbean [3, 37, 40]. Here we analyzed the type of P. areolata (USNM 8443), Smittina areolata, holotype, F. Canu & R. Bassler det., Molokai, Hawaii, 142–406 m, coll. 1902, Fig 3A–3D), revealing that this species is not conspecific with the Brazilian material. Parasmittina areolata has a double row of areolar pores (single in specimens from Brazil), low secondary orifice (with lateral flaps in Brazilian material) and ectooecium centrally perforated (distally perforated in specimens from Brazil). The morphologically related species P. spathulata is distinct from the Brazilian material in having a broader lyrula (acc. Winston [7]). Specimens from the Caribbean previously attributed to P. areolata by Winston [37] were reassigned to P. luteoserrula Winston & Jackson, 2021 (see Winston & Jackson [13]), distinct from Brazilian specimens by having an orifice with a serrated distal margin, and a large avicularium with a coarsely serrated margin.

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Fig 3. Parasmittina areolata (Canu & Bassler, 1927) (A–D) USNM 8443, holotype, Hawaii, USA.

Arrows indicating avicularia. (A) group of autozooids and ovicelled zooids, (B) detail of autozooid with small avicularia, (C) detail of primary orifice, (D) detail of ovicelled zooids with small and large avicularia. Scale bars: A = 400 μm; B = 100 μm; C = 50 μm.

https://doi.org/10.1371/journal.pone.0304347.g003

Specimens studied here shares most of the diagnostic characters provided by Ramalho et al. [11] in the description of P. abrolhosensis, including a primary orifice with distal margin smooth, lyrula narrow and robust and down-curved hooked condyles with serrated margins; secondary orifice with a U-shaped pseudosinus; avicularia with four morphologies: (1) small, narrow and elongate, (2) small, subtriangular and bulbous [not described by Ramalho et al. [11], but figured in 3H], (3) small, narrow and subtriangular to elliptic, and (4) large spatulate; and ovicells densely surrounded by adjacent frontal wall in older colonies, and with small pseudopores. However, specimens from Ramalho et al. [11] have 3–4 oral spines (1–3 in colonies studied here) and the large avicularium was not found as vicarious. Interestingly, the original description of P. abrolhosensis was based on three small colonial fragments inhabiting corals (acc. Ramalho et al. [11], Figs 3H, 4A–4D) whereas several colonies studied here are from artificial substrata and material from Canu & Bassler [40] are colonies with rough secondary calcification. Since the number of oral spines and occurrence of avicularia in Parasmittina are very variable in relation to colony development and habitat (e.g., [2, 4, 5, 9, 21, 39]), these differences are likely to be intraspecific variations of P. abrolhosensis rather than a different species.

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Fig 4. Parasmittina alba Ramalho, Muricy & Taylor, 2011.

(A–B) UFBA 5059, Bahia, Brazil. Arrows indicating avicularia. (A) ancestrula and first zooids of the colony, (B) young autozooids showing small avicularium. (C–D) UFBA 5009, Bahia, Brazil. (C) detail of primary orifice, (D) group of young autozooids showing large avicularium, (E) UFBA 5010, Bahia, Brazil, colony with secondary calcification showing autozooids and ovicelled zooids, (F) UFPE 785, Espírito Santo, Brazil, detail of ovicelled zooids with small avicularia. Scale bars: A, B, D, E, F = 200 μm; C = 50 μm.

https://doi.org/10.1371/journal.pone.0304347.g004

Distribution.

SW Atlantic: Brazil (Canu & Bassler [32]; Vieira et al. [25]; Almeida et al. [26]; Ramalho et al. [11]; present study).

Material examined.

UFPE 785, Ilhas Rasas, Guarapari, Espírito Santo, Brazil, 11–15 m, coll. 27/03/2017; UFPE 786–795; UFBA 5009–5010, 5013, 5016, 5027, 5033, 5036, 5041, 5045, 5047, 5054, 5058, 5062, 5065, 5069, 5074, 5079, 5084, 5088, 5098–5099, 5103, 5108–5109, 5120–5121, 5123, 5141–5142, 5148, 5156, 5165–5166, 5172, 5175, 5178, 5189, 5194, 5202–5203, 5207, 5210, 5215, 5221, 5228, 5235, 5240, 5246, 5251, 5257, 5263–5264, 5273–5274, 5281–5182, 5285, 5290, 5303, 5355, 5425, 5448, Baia de Todos os Santos, Salvador, Bahia, Brazil, 3–5 m, coll. 2012, MZUSP 2937, Alcatrazes, São Sebastião, São Paulo, Brazil, coll, 06/10/2011.

Description.

Colony encrusting. Ancestrula (Fig 4A) tatiform, with narrow marginal cryptocyst, 8 marginal spines; 4–5 orificial spines in first daughter zooid; second and third daughter zooids with 3–4 orifical spines. Autozooids (Fig 4B) subrectangular, limited by slightly raised lateral walls, surrounded by a single row of 20–27 marginal pores (0.010–0.019–0.032 mm in diameter; n = 30; SD = 0.005 mm). Frontal wall rugose, with small, rounded tubercles. Primary orifice (Fig 4C) elliptical, distal margin smooth, with 1–3 oral spines; lyrula broad (0.038–0.046–0.058 mm wide; n = 15; SD = 0.005 mm), but shallow and often with a median keel; condyles paired, thin, with smooth margins and down-curved hooked tips. Secondary orifice (Fig 4E and 4F) raised around the proximal margin of the primary orifice, formed from lateral flaps, resulting in a shallow V-shaped pseudosinus. Adventitious avicularia variable in shape and size (Fig 4B, 4D and 4F), with three morphologies: (1) small, narrow, and subtriangular avicularia (Fig 4B and 4F), rare in very young zooids, placed laterally at one side of the orifice, commonly proximally oriented, rostrum subtriangular, finely serrated at its lateral margins, pointed tip, palate narrow and subtriangular foramen; (2) small and spatulate avicularia with broad rostrum (Fig 4F), rare in young zooids, placed laterally at one side of the orifice, proximally oriented, rostrum subspatulate, a rounded distal edge, palate narrow and elliptical foramen; (3) large spatulate avicularia (Fig 4D), more common in older zooids, placed laterally at one side of the orifice, oriented proximally, with a rounded distal edge, palate broad, foramen elliptical, with smooth margins and a complete crossbar, with 2–3 pseudopores adjacent to the avicularia. Ovicells (Fig 4E and 4F) surrounded by the frontal wall of adjacent zooids, becoming immersed in older colonies; ooecium almost globular with a flattened frontal surface (0.007–0.018–0.045 mm in diameter; n = 30; SD = 0.007 mm), ectooecium with 18–26 funnel-shaped pseudopores that become merged and polygonal with increasing calcification.

Remarks.

Parasmittina alba was described based on specimens from Rio de Janeiro, SE Brazil; it was characterized by having a granular frontal wall, condyles with hooked tips, large lyrula, 1–2 oral spines, secondary orifice with lateral projections and pseudosinus, avicularia latero-oral (small subtriangular or rounded), large (spatulate) and interzooidal (subtriangular), with only one avicularium occurring per zooid, and ectooecium with pseudopores [10]. Most of these morphological characters are also seen in colonies from SE and NE Brazil examined here, despite the presence of 1–3 orificial spines and the rare presence of interzooidal avicularia. Most of our examined material form small patches growing on ceramic experimental tile plates (specimens from northeastern Brazil; Fig 4A), but the larger specimens have been only observed growing on rhodoliths (specimens from southeastern Brazil; Fig 4F). The avicularia were often found in older part of the colonies (Fig 4F) when comparing with the growing zone with the new zooids (Fig 4B), suggesting the formation of the avicularia in later colony astogeny. Moreover, we found no morphometric differences in colonies studied here assigned and other records of P. alba (Table 2).

Parasmittina alba was reported as a non-indigenous species in Portugal, Northeastern Atlantic [17]. Souto et al. [17] noted slight variations between specimens from Rio de Janeiro (acc. Ramalho et al. [10]) and those from Portugal, including smaller ectooecial pseudopores related with more significant calcification, the occurrence of two avicularia in ovicelled zooids and absence of interzooidal avicularia. Additionally, Souto et al. [17] suggested that P. alba could be assigned as a junior synonym of P. betamorphaea Winston, 2005 [7] described from the United States (Northwestern Atlantic) since characters used to distinguish these taxa are very variable among colonies and zooids (i.e., number of avicularia, calcification of margins and rostrum of the avicularia). The Caribbean P. lavela Soule & Soule [5] also shares most morphological diagnostic features of P. alba. These taxa have a granular frontal calcification, primary orifice without distal denticles, with large lyrula and thin down-curved hooked condyles, secondary orifice with a short pseudosinus, and ooecium with merged pseudopores [5]. The only difference between P. alba and P. lavela is the presence of a single morphotype of avicularia in P. lavela (i.e., small subtriangular latero-oral avicularia), lacking all other types described to P. alba. Soule & Soule [9] stated that avicularia are not common in P. lavela, but only a tiny single specimen growing on algae on an anchor chain was examined [5], somewhat corroborating morphological variation and biological associations already reported [10, 17] and assigned here to P. alba. Avicularia are known to be very variable in Smittinidae according to colony development and habitat (e.g., [2, 4, 5, 9, 21, 39]). Avicularia morphology is quite variable in specimens of P. alba here examined. We suspect that P. alba and P. betamorphea may represent different astogenetic variations of P. lavela–specimens of P. alba comprising a stage with all types of avicularia, ovicells, and secondary calcification [10], whereas P. betamorphea could represent young colony that lacks ovicells and have few avicularia [7].

Zooidal measurements of specimens attributed to P. alba and P. betamorphea are like those of P. lavela (Table 2). In addition, a peculiar feature of the species (as already mentioned by Souto et al. [17]) is a notch on the distal margin of the primary orifice of ovicellate zooids–this notch is formed in the place where the oral spines were inserted (Fig 4E) [see Ramalho et al. [10] (Fig 2G) and Souto et al. [17] (Fig 3B)]. However, observing this notch in colonies of P. lavela and P. betamorphea was impossible. Ovicelled zooids of P. lavela had the distal margin of the primary orifice occluded by secondary calcification [5] and P. betamorphea lacks ovicells [7]. Thus, at least one species complex involving P. alba, P. betamorphea, and P. lavela can be recognized (Table 2).

Finally, another congener may be involved in this complex. Specimens from the Southeast and Northeast Atlantic, as well as from the Mediterranean attributed to Parasmittina protecta (Thornely, 1905) (acc. Harmelin et al. [9]) also share most morphological diagnostic features of P. alba, being only variable in avicularia morphotypes occurrence. However, P. protecta was first described with colonies from the Indian Ocean and the original description is brief, not including diagnostic features of the primary orifice (distal margin ornamentation, condyles, lyrula) and detailed characterization of avicularia (acc. Thornely [43]). Also, there is no redescription of type or topotype specimens, preventing us from reliably characterizing P. protecta from Thornely (1905). Additional studies including more specimens are required to identify whether P. protecta and P. alba belong to the same species.

Distribution.

Northeastern Atlantic: Portugal [17]; SW Atlantic: Brazil [10] present study).

Material examined.

UFBA 946, Baía de Todos os Santos, Bahia, Brazil, coll. 1997; UFBA 3113, Costa do Dendê, Bahia, Brazil, coll. 2002.

Description.

Colony encrusting. Autozooids (Fig 5A) subrectangular to polygonal, limited by slightly raised lateral walls, with a single row of 18–24 marginal pores (0.009–0.019–0.033 mm wide; n = 30; SD = 0.005 mm). Frontal wall rugose, with large, rounded tubercles. Primary orifice (Fig 5C) transversely elliptical, distal margin smooth, with 1–2 oral spines; lyrula narrow (0.019–0.025–0.032 mm wide; n = 15; SD = 0.004 mm), latero-proximal condyles triangular and thin. Secondary orifice initially low, becoming raised and forming lateral flap-shaped projections with increasing calcification, often with a shallow U-shaped pseudosinus (Fig 5D), partially obscuring primary orifice in latter astogeny, especially in ovicelled zooids, resulting in a deep U-shaped pseudosinus, but often not obscuring the lyrula (Fig 5E). Adventitious avicularia variable in shape and size (Fig 5A–5E), with three morphologies: (1) small, subtriangular, bulbous avicularia (Fig 5A and 5B), placed laterally at one side of the orifice, proximally oriented, rostrum subtriangular, corrugated at its lateral margins, pointed tip, palate narrow and subtriangular foramen; (2) small, oblong to spatulate avicularia (Fig 5A and 5B) single, common in younger zooids, placed below the secondary orifice, proximally oriented, rostrum subspatulate and straight, smooth at its lateral margins, rounded tip, palate occupying about half of the rostrum length and elliptical foramen; (3) large, sublanceolate avicularia (Fig 5A), placed laterally at one side of the orifice, oriented proximally, with acute rostrum, palate broad, foramen subtriangular, with finely serrated margins and crossbar complete, with 2–3 pseudopores adjacent to the avicularia. Large frontal avicularia (Fig 5A and 5B) occasionally present, with the same morphology as the latero-oral. Ovicells (Fig 5E–5F) wider than long, ooecium globular, becoming immersed in the frontal calcification with increasing calcification (Fig 5F); ectooecium with 20–27 pseudopores with slightly raised rim (0.004–0.011–0.020 mm wide; n = 30; SD = 0.004 mm).

Remarks.

Parasmittina bimucronata is characterized by having the primary orifice smooth distally, 1–2 oral spines, thin and smooth condyles and lyrula occupying one-quarter of the orificial width; adventitious latero-oral avicularia with two sizes and three morphologies: small (with subtriangular or oblong profile) and large (with sublanceolate profile); and ovicells with more than 18 pseudopores (description based on lectotype, BMNH 1899.5.1.920; see Hayward & Parker [45], Fig 6D–6E). There are no morphological differences between Brazilian specimens studied here and the lectotype of P. bimucronata (see comparison in Table 3).

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Fig 6. Parasmittina dubitata Hayward, 1980.

(A–D) Uncatalogued specimen, Tierra del Fuego, Argentina. Arrows indicating avicularia. (A) group of autozooids showing small and large avicularia, (B) detail of autozooids with small oblong and large subtriangular avicularia, (C) detail of primary orifice, (D) detail of vicarious and small spatulate avicularia. Scale bars: A = 200 μm; B, D = 100 μm; C = 50 μm.

https://doi.org/10.1371/journal.pone.0304347.g006

Parasmittina bimucronata was originally described based on specimens from the Indian Ocean as a variation of P. trispinosa [44], and the lectotype of that species was selected by Hayward & Parker [47]. Morphological differences can be observed between these two species, including: number of oral spines (1–2 in P. bimucronata and 2–3 in P. trispinosa), orientation of the large avicularium (proximolateral in P. bimucronata and distolateral in P. trispinosa), and number of ectooecial pseudopores (20–37 in P. bimucronata and 2–4 in P. trispinosa) [5, 47]. Hincks [48] referred to specimens from the Pacific Ocean as belonging to P. bimucronata. However, later, Harmer [36] relocated specimens from Indian and Pacific Oceans studied by Hincks [44, 48] to P. raigii (Audouin, 1826), originally described from the Red Sea (Gulf of Suez as the type locality). Hayward & Parker [47] reexamined Hincks’ [47, 49] original specimens and stated that none of them belonged to P. raigii—specimens from the Indian Ocean belong to P. bimucronata and those from the Pacific were renamed as a new species, P. pectinata Hayward & Parker, 1994 [47]. Although P. bimucronata, P. raigii and P. pectinata have adventitious avicularia placed laterally to the orifice with similar morphologies, these species can be distinguished mainly by features of the primary orifice, including the distal margin (smooth in P. bimucronata; beaded in P. raigii and P. pectinata), oral spines (1–2 in P. bimucronata and P. raigii; 2–3 in P. pectinata), condyles (thin and smooth in P. bimucronata and P. raigii; robust and serrated in P. pectinata) and lyrula size (narrow in P. bimucronata; broad in P. raigii and P. pectinata). Liu [45] also assigned specimens from China to P. glomerata due to avicularia with similar morphologies. However, these specimens are here attributed to P. bimucronata, since it differs from P. glomerata by having a primary orifice with smooth distal margin (beaded in P. glomerata) and narrow lyrula (medium-sized in P. glomerata).

Distribution.

Indo-Pacific: Myanmar and China [44, 45]; SW Atlantic: Brazil (present study).

Parasmittina dubitata Hayward, 1980.

(Fig 6; Table 10)

Parasmittina dubitata Hayward, 1980: 701, figures 2A–B [49].

Material examined.

Uncatalogued, Tierra del Fuego, Argentina, 90 m.

Description.

Colony encrusting. Autozooids (Fig 6A), (0.305–0.403–0.545 mm length; n = 8; SD = 0.096 mm; 0.215–0.267–0.382 mm wide; n = 8; SD = 0.049 mm), subrectangular to polygonal, limited by slightly raised lateral walls, with a single row of 11–16 marginal pores (0.013–0.029–0.059 mm wide; n = 30; SD = 0.010 mm). Frontal wall rugose, with large, rounded tubercles. Primary orifice (Fig 6C), (0.093–0.103–0.120 mm length; n = 7; SD = 0.008mm; 0.086–0.108–0.123 mm wide; n = 7; SD = 0.011mm), subcircular, distal margin smooth, with single oral spine; lyrula large, varying in size, occupy about half width of the orifice (0.034–0.041–0.049 mm wide; n = 7; SD = 0.005 mm), robust, with concave distal margin; a pair of prominent condyles with rounded and coarsely serrated margins. Secondary orifice cormidial, low, forming slightly raised side flaps and a hood distal to the orifice (Fig 6B). Adventitious avicularia variable in shape and size (Fig 6B and 6D), with three morphologies: (1) small (0.059–0.099–0.131 mm length; n = 15; SD = 0.022; 0.017–0.031–0.046 mm wide; n = 15; SD = 0.008 mm), oblong to spatulate avicularia (Fig 6A and 7B) single or paired, laterally at one side of the orifice and oriented proximally or placed near zooidal margins, smooth at its lateral margins, rounded tip, palate occupying one quarter of the rostrum length and elliptical foramen; (2) (0.056–0.066–0.073 mm mm length; n = 4; SD = 0.007; 0.026–0.029–0.033 mm wide; n = 4; SD = 0.003 mm), small, spatulate avicularia (Fig 6A and 6D), placed in zooidal margins, commonly replacing a marginal pore; (3) large (0.241mm in length; n = 1; 0.123 mm in wide; n = 1), subtriangular to sublanceolate avicularia (Fig 6B) (0.425 mm in length; 0.025 mm in wide; n = 1), placed laterally at one side of the orifice, oriented proximally, with acute rostrum, palate broad, foramen elliptical, with smooth margins and crossbar complete. Vicarious avicularia (Fig 6D) with rostrum shorter than autozooids (0.266 mm in length; n = 1; 0.110 mm in wide; n = 1), with the same morphology as the large adventitious avicularium, randomly oriented. Ovicells not observed.

Remarks.

Parasmittina dubitata was first described based on specimens from Burdwood Bank, Argentina, growing on organic carbonates [49]. Here, we provide characterization of a single specimen from Tierra del Fuego, Argentina, kindly sent by Juan Lopez Gappa (pers. comm. 2021), that exhibts the diagnostic characters of the original description of P. dubitata. This species is readily distinguished from other congeners by the primary orifice morphology, including a lyrula with a concave distal margin and rounded condyles, unlike the straight lyrula and triangular to hooked condyles of most Parasmittina species.

Distribution.

SW Atlantic: Argentina (Burdwood Bank and Tierra del Fuego) [49] present study).

Material examined.

Holotype: NHMUK 2023.9.22.1, Smittia trispinosa var. ligulata, S.O. Ridley det., Alert Circumnavigation 1878–1882, HMS Alert, Victoria Bank, Espírito Santo, Brazil, 60 m.

Redescription.

Colony encrusting. Autozooids (0.324–0.458–0.603 mm length; n = 15; SD = 0.073 mm; 0.209–0.324–0.462 mm wide; n = 15; SD = 0.072 mm), (Fig 7A) polygonal, almost rhombic, limited by slightly raised lateral walls, surrounded by a single row of 19–27 marginal pores (0.010–0.019–0.032 mm in diameter; n = 30; SD = 0.004 mm). Frontal wall with rugose and nodular calcification (Fig 7A). Primary orifice (0.063–0.093–0.112 mm length; n = 4; SD = 0.023 mm; 0.074–0.087–0.096 mm wide; n = 4; SD = 0.009 mm) (Fig 7C) elliptical, distal margin smooth, oral spines not observed, lyrula narrow (0.015–0.021–0027 mm wide; n = 4; SD = 0.005 mm); a pair of robust and down-curved hooked condyles with coarsely serrated margins (Fig 7B). Secondary orifice (Fig 7B and 7F) pear-shaped, forming lateral flaps, resulting in a shallow U-shaped pseudosinus (Fig 7E and 7F). Adventitious avicularia variable in shapes and sizes (Figs 7B, 7D and 7F), with three morphologies: (1) small, narrow, and elongated avicularia (Fig 7B, 7D and 7F) (0.108–0.163–0.210 mm in length; n = 10; SD = 0.034 mm; 0.015–0.022–0.032 mm in wide; n = 10; SD = 0.005 mm), present at one or both side of the orifice, unequal in size if paired, placed below the secondary orifice, proximally oriented, rostrum narrow and slightly curved, smooth to slightly corrugated at its lateral margins, rounded tip, palate occupying about half of the rostrum length and oblong foramen; (2) small, narrow and elliptic avicularia (Fig 7B and 7F) (0.060–0.083–0.116 mm in length; n = 10; SD = 0.014 mm; 0.013–0.017–0.025 mm in wide; n = 10; SD = 0.003 mm), placed o zooidal margins and/or o the frontal wall, with smooth lateral margins, rounded tip, palate narrow and elliptical foramen; (3) large, sub-lanceolate avicularia (Fig 7D), placed laterally at one side of the orifice, oriented proximally, rostrum slightly curved with rounded distal edge, palate narrow and calcified, occupying more than half of avicularium chamber, foramen elliptical, crossbar complete, without columella, Ovicells (0.171–0.185–0.211mm length; n = 5; SD = 0.017 mm; 0.163–0.188–0.212 mm wide; n = 5; SD = 0.022 mm) globose, densely surrounded by adjacent frontal wall, ectooecium with 6–10 medium–sized pores (Fig 7F).

Remarks.

Parasmittina ligulata comb. nov. belongs to the complex P. spathulata–P. areolata, that comprise taxa from the Atlantic and Pacific Oceans with single or paired adventitious latero-oral avicularia with narrow and elongated profile (e.g., [3, 7, 21]).

Parasmittina ligulata comb. nov. was originally described based on specimens from southeastern Brazil, but later synonymized under P. spathulata by Vieira et al. [25], who also include in the same synonym list Brazilian specimen attributed to Smittina trispinosa spathulata (USNM 8558). As stated above, the specimen studied by Canu & Bassler [40] belongs to P. abrolhosensis. Also, the analysis of the syntype showed that P. ligulata comb. nov. can be readily differentiated from P. spathulata and P. abrolhosensis by showing large, avicularia elongate to sublanceolate avicularia (spatulate in the other species). Other differences between P. ligulata comb. nov. and P. spathulata is lyrula size (occupying one-quarter of the orifice in P. ligulata comb. nov. and half of the orifice in P. spathulata), and between P. ligulata comb. nov. and P. abrolhosensis is the occurrence of small latero-oral subtriangular avicularia in P. abrolhosensis (absent in P. ligulata comb. nov.).

Among all congeners, P. ligulata comb. nov. most resembles Parasmittina longirostrata Liu in Liu, Yin & Ma, 2001 [45] mainly because of small proximolateral, elongate and large sublanceolate avicularia. However, these species are distinguished by lyrula size (occupying about one-quarter of the orifice in P. ligulata comb. nov. and half of the orifice in P. longirostrata) and small oblong avicularia (absent in P. ligulata comb. nov. and very common in P. longirostrata).

Distribution.

SW Atlantic: Brazil [50].

Material examined.

UFPE 816–821, UFBA 5030, 5097, 5198, 5213, 5248, 5297, 5343, 5349, 5354, 5360, 5365–5366, 5370–5372, 5374, 5389, 5396, 5400, 5407, 5409, 5414, 5416, 5422, 5427, 5430, 5431, 5436, 5438, 5444, 5453, 5465, Baia de Todos os Santos, Salvador, Bahia, Brazil, 3–5 m, coll. 2012.

Description.

Colony encrusting (Fig 8A). Autozooids (Fig 8B) subrectangular to polygonal, limited by slightly raised lateral walls, surrounded by a single row of 12–18 small marginal pores (0.004–0.013–0.025 mm in diameter; n = 30; SD = 0.004 mm). Frontal wall rugose and nodular. Primary orifice elliptical (Fig 8C), wider than long, distal margin smooth, with 3–4 oral spines, lyrula median-sized (0.025–0.030–0.036 mm wide; n = 15; SD = 0.003 mm), a pair of robust, hooked, condyles with serrated margins (up to seven teeth). Secondary orifice (Fig 8D and 8F) moderate to well-developed, pear-shaped, forming 2–4 lateral flaps commonly resulting in a shallow U-shaped pseudosinus in autozooids, only partly obscuring the lyrula, with a hood-shaped distal calcification in ovicelled zooids. Adventitious avicularia variable in shapes and sizes (Fig 8B–8D), with two morphologies: (1) small, narrow and elongate avicularia (Fig 8B and 8D) present at one side below to the secondary orifice, proximally oriented, rostrum narrow and slightly curved, slightly corrugated at its lateral margins, rounded tip, palate occupying about half of the rostrum length, oblong foramen and crossbar complete; (2) large, sub-lanceolate avicularia (Fig 8C and 8E), placed laterally at one side of the orifice, oriented proximally, rostrum slightly curved with coarsely serrated margins and rounded distal edge, palate narrow, occupying about half the rostrum length, foramen subtriangular with 2–3 pseudopores adjacent to the avicularia. Ovicells globose, initially prominent (Fig 8D, and 8F) and densely surrounded by adjacent frontal wall (Fig 8F) in older zooids; ectooecium with 18–24 medium-sized pseudopores (0.003–0.006–0.009 in diameter; n = 30; SD = 0.001 mm), regularly distributed through the ectooecial surface.

Remarks.

Parasmittina longirostrata is characterized by the combination of a primary orifice with smooth distal margin, with 3–4 oral spines, lyrula median-sized, secondary orifice forming a U-shaped pseudosinus, and two types of proximolateral avicularia: small, elongate and thin, and large, sub-lanceolate with crenulated margins [45].

Liu et al. [45] considered that P. serrula Soule & Soule, 1973 [2] was the most similar congener to P. longirostrata probably because of having two types of avicularia with the smaller and proximolateral being thin and narrow. However, several differences are observed between these species, including the primary orifice (with smooth distal margin and lyrula occupying half of the orificial width in P. longirostrata and with distal denticles and lyrula occupying one-quarter of the orificial width in P. serrula), placement of the smaller avicularia (typically straightly placed proximolateral to the orifice in P. longirostrata and transversally below the orifice in P. serrula) and profile of the large avicularium (sublanceolate in P. longirostrata and lanceolate with lobate edge at half distal part in P. serrula). A congener very similar to P. longirostrata, however, is P. serruloides Harmelin et al. 2009 [9], described based on specimens from the Mediterranean. These species are only distinguished by the profile of the condyles (robust and with 4–7 teeth in P. longirostrata, but thin and with 2–5 teeth in P. serruloides). However, the profile of the condyles can be variable within a colony, as already seen in other Parasmittina (e.g., P. onychorrhyncha Ryland & Hayward, 1992 and P. aleutensis Soule & Soule, 2002). Thus, despite the type locality of P. longirostrata being in the North Pacific. The morphology and morphometry of the specimens from Brazil resemble those of specimens of P. longirostrata from China [45], but the autozooids of P. serruloides appear to be smaller zooids when compared with P. longirostrata (Table 4). However, further studies are needed with specimens from the Mediterranean, to determine if there are intraspecific differences that justify the synonymization of P. serruloides with P. longirostrata

Distribution.

Northeastern Pacific: China [45]; SW Atlantic: Brazil (present study). Specimens from Lebanon [9] need to be compared to ascertain the synonym with P. longisrostrata.

Parasmittina pinctatae Liu in Liu, Yin & Ma, 2001.

(Figs 9, 10; Tables 5, 10)

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Fig 9. Parasmittina pinctatae Liu in Liu, Yin & Ma, 2001.

(A–C) UFBA 5447, (D–F) UFBA 5453, Bahia, Brazil. Arrows indicating avicularia. (A) ancestrula and first zooids of the colony, (B) young autozooids showing small and large avicularia, (C) detail of primary orifice and small avicularium, (D) group of autozooids showing small avicularia, (E) detail of autozooids and large avicularium, (F) autozooids and ovicelled zooids. Scale bars: A, B, D–F = 250 μm; C = 50 μm.

https://doi.org/10.1371/journal.pone.0304347.g009

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Fig 10. Parasmittina pinctatae Liu in Liu, Yin & Ma, 2001.

(A–D, F) UFBA 5204, (C, E) UFBA 5466, Bahia, Brazil. Arrows indicating avicularia. (A) general view of a colony, (B) autozooids at the growing edge of the colony showing small avicularia, (C) detail of primary orifices, (D) detail of primary orifice with small avicularia, (E) group of autozooids with small and large avicularia, (F) group of ovicelled zooids with secondary calcification. Scale bars: A, F = 500 μm; B, D = 200 μm; C = 100 μm; E = 400 μm.

https://doi.org/10.1371/journal.pone.0304347.g010

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Table 5. Morphometric data of P. pinctatae, P. parsevalii and P. egyptiaca.

Values given in millimeters and represented as minimum–median–maximum (number of zooidal measures), (*) = In Liu et al. (2001) there is an error in the median value, which is why it was adopted this way Avicularia abbreviations: Av1 = small subtriangular; Av2 = small elongate; Av3 = large spatulate.

https://doi.org/10.1371/journal.pone.0304347.t005

Parasmittina pinctatae Liu in Liu, Yin & Ma, 2001: 805, plate 58, figures 3–6 [45].

Smittina trispinosa: Luederwaldt 1929: 65 [49]. Non Discopora trispinosa Johnston, 1838: 280 [51].

Smittina trispinosa var. nitida: Marcus 1937: 104, plate 21, figure 56 [23]. Non Discopora nitida Verril, 1875: 415 [51].

Parasmittina betamorphaea: Vieira et al. 2008: 27 [25]. Non Parasmittina betamorphaea Winston, 2005: 58 [7].

Parasmittina parsevalii: Liu et al. 2001: 621, plate 54, figures 5–7 [46]. Non Cellepora parsevalii Audouin, 1826: 238 [5].

Parasmittina egyptiaca: Harmelin et al. 2009: 166, fig 2A–2E [9]; Baradari et al. 2019: 474, figures 54–57 [18]. Non Smittia egyptiaca Waters, 1909: 157 [52].

Material examined.

UFBA 301, 644, 1112, 5466, Todos os Santos, Bahia, Brazil, 37 m, coll. 17/04/1997; UFBA 5317, Praia do Francês, Marechal Deodoro, Alagoas, Brazil, coll. 03/02/2003; UFPE 2787, Porto do Cabedelo, Cabedelo, Paraíba, Brazil, intertidal, coll. 27/09/2009; UFPE 2582–2583, Praia Araçá, São Sebastião, São Paulo, Brazil, coll. 07/07/2009; USNM Uncatalogued, H. Luederwaldt det. 1926, Ilha de São Sebastião, São Paulo, Brazil; UFPE 822–830, UFBA 5011, 5022, 5025, 5031, 5039, 5050, 5055, 5059, 5066, 5070, 5075, 5080, 5085, 5089, 5094, 5100, 5104, 5110, 5116, 5127, 5130, 5136, 5144, 5151, 5157, 5168, 5177, 5193, 5195, 5204, 5216, 5223, 5230, 5236, 5241, 5245, 5252, 5259, 5260, 5265, 5270, 5278–5279, 5287, 5291, 5298, 5345, 5351, 5358, 5363, 5373, 5384, 5386, 5397, 5417, 5424, 5428, 5451, 5454, 5457, 5461, 5466, 5497, 5503, 5506–5507, Baia de Todos os Santos, Salvador, Bahia, Brazil, 3–5 m, coll. 2012; MZUSP 921, Smittina trispinosa var. nitida, det. Marcus, 1937, no locality [supposedly Santos, São Paulo, Brazil]; MZUSP 1160, Iate Clube Ilhabela, Ilhabela, São Paulo, Brazil, 2 m, coll. 05/03/2010; MZUSP 2430.3, CE59, Porto do Mucuripe, Fortaleza, Ceará, Brazil, coll. 27/08/2009; MZUSP 2952, CE65, Porto do Mucuripe, Fortaleza, Ceará, Brazil, 3°32’S, 38°48’W, coll. 27/08/2009; MZUSP 2420, 2431.1, CE67, Porto do Mucuripe, Fortaleza, Ceará, Brazil, coll. 27/08/2009; MZUSP 2953, CE69, Porto do Mucuripe, Fortaleza, Ceará, Brazil, coll. 27/08/2009; MZUSP 2515, Ubatubinha, Ilha Grande, Angra dos Reis, Rio de Janeiro, Brazil,… . coll, 15/10/2012; MZUSP 1015, Smittina trispinosa var. nitida, det. Marcus, 1937, no locality [supposedly Santos, São Paulo, Brazil]; USNM Uncatalogued, Smittina trispinosa, det. H. Luederwaldt, São Sebastião, São Paulo, Brazil, coll. Jul 1925.

Description.

Colony encrusting, uni to multilaminar (Fig 9A). Ancestrula (Fig 9A) tatiform, without marginal cryptocyst, 1 marginal spine; 3 orificial spines in first daughter zooid. Autozooids (Figs 9B, 10B) subquadrangular to polygonal, limited by slightly raised lateral walls, surrounded by a single row of 16–22 marginal pores (0.011–0.022–0.032 mm in diameter; n = 30; SD = 0.004 mm). Frontal wall rugose and nodular. Primary orifice (Figs 9C and 10C) subcircular, as long as wide, smooth distally, 1–2 oral spines, lyrula relatively wide but low, occupying about half of the orifice length (0.025–0.038–0.047 mm wide; n = 15; SD = 0.006 mm), a pair of almost straight and robust condyles with fine serrated margins. Secondary orifice low, forming short lateral flaps (Figs 9D, 10C), larger in ovicelled zooids (Figs 9F, 10F). Adventitious avicularia variable in shape and size (Fig 9B–9D), with three morphologies: (1) small subtriangular avicularia (Figs 9B and 10B, 10E), placed distolaterally to the orifice in younger zooids and randomly scattered on the frontal wall (i.e., around the orifice, and on the ovicell) in older zooids (Fig 10F); (2) small, profile elongate, sublanceolate (Figs 9C, 9E and 10C), to spatulate (Fig 10C), narrow and with pointed rostrum, placed o zooidal margins, more common in older zooids; (3) large, profile spatulate (Figs 9B, 9E and 10E), placed distolaterally to the orifice, oriented proximolaterally, palate narrow, occupying about three-quarters of the rostrum length, with smooth margins and crossbar complete; 3–5 pseudopores adjacet to the avicularia, foramen elliptical. Ovicells globose (Figs 9F and 10F), densely surrounded by adjacent frontal wall (Fig 10F); ectooecium with more than 20 small to medium-sized pseudopores (0.002–0.007–0.011 in diameter; n = 30; SD = 0.002 mm) distributed through the entire ovicell surface.

Remarks.

Although P. pinctatae occurs in Brazil since at least 1929, due to misleading identifications [23, 26, 53], we present the first formal record of this species to the Western Atlantic. In Brazil, this species was previously attributed to P. trispinosa [32, 53], and P. nitida (Verrill, 1875) but Vieira et al. [25] misassigned Marcus’s P. nitida to P. betamorphaea. Here we examined specimens studied by several authors (Luederwaldt [53], USNM Uncatalogued; Marcus [23], MZUSP 921; Almeida et al. [26], UFBA 301 and UFBA 644), and all share with P. pinctatae the subcircular primary orifice, secondary orifice with lateral flaps, short lyrula, nodular frontal calcification and three types of avicularia. Additionally, specimens recently assigned to P. egyptiaca by Orr et al. [54] from Brazil (Bahia) and Spain belong to P. pinctatae (Table S2 of supplementary material from [54]).

Parasmittina pinctatae differs from P. trispinosa in the profile of the primary orifice (as long as wide in P. pinctatae and longer than wide in P. trispinosa), number of oral spines (1–2 in Parasmittina pinctatae and 2–3 in P. trispinosa), profile of avicularia (the proximolateral is subtriangular in P. pinctatae and oblong in P. trispinosa; the large is spatulate in P. pinctatae and subtriangular in P. trispinosa), and number of ovicell pseudopores (more than 20 in P. pinctatae and 2–4 in P. trispinosa) [5]. Differences between P. pinctatae and P. nitida include the profile of the primary orifice (subcircular in P. pinctatae and rounded in P. nitida), lyrula (median in P. pinctatae and narrow in P. nitida), types of avicularia (three types in P. pinctatae: proximolateral, marginal and large; two types in P. nitida: proximolateral and marginal) and orientation of the proximolateral avicularia (distolateral in P. pinctatae and proximolateral in P. nitida) [55]. Finally, P. pinctatae is distinguished from P. betamorphea in having a narrower lyrula (the lyrula of P. betamorphaea is twice the length of that from of P. pinctatae) and condyles thin and almost straight (robust and curved in P. betamorphaea) [7].

The taxonomic history of P. pinctatae needs to be explained. Liu et al. [45] attributed other specimens from China to P. parsevalii (Audouin, 1826) due to these having avicularia placed at the frontal wall and laterally to the orifice (not associated with the peristome like in P. pinctatae) and differences in ooecia surface. However, P. parsevalii sensu Liu et al. [45] differs from P. parsevalii (acc. Hayward & Parker [47]) by having a primary orifice with smooth distal margin (beaded in P. parsevalii), relatively wide and low lyrula (narrow and high in P. parsevalii), almost straight and thin condyles (robust and hooked in P. parsevalii) and large spatulate avicularia (subtriangular in P. parsevalii). Thus, here we reassign the Chinese specimens of P. parsevalii to P. pinctatae.

Some records of P. egyptiaca made by Harmelin et al. [9, 56] and Baradari et al. [18] also belong to P. pinctatae. The type specimen of P. egyptiaca (MFN Uncatalogued; Fig 11) is distinct from specimens characterized by these authors by having a raised secondary orifice, large avicularia with subtriangular profile and serrated margins and latero-oral avicularia oriented proximally. Thus, a review of specimens previously attributed to both P. parsevalii and P. egyptiaca and morphologically related is strongly recommended.

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Fig 11. Parasmittina egyptiaca (Waters, 1909).

(A–F) MFN 1143, type. Arrows indicating avicularia. (A) colony fragment showing small and large avicularia, (B) detail of autozooid showing oral spines and small avicularia, (C) detail of autozooid showing large avicularia, (D) detail of primary orifice showing condyles and lyrula, (E) detail of primary orifice showing oral spines and slightly denticulate distal margin, (F) detail of ovicell. Scale bars: A = 300 μm; B, C, F = 100 μm; D, E = 20 μm.

https://doi.org/10.1371/journal.pone.0304347.g011

Distribution.

Central Pacific: China [45]; Red Sea [52]; Mediterranean: Lebanon [9, 56]; Persian Gulf: Iran [18]; SW Atlantic: Brazil [26, 23, 53] present study).

Material examined.

UFBA 2850, Guarajuba, Camaçari, Bahia, Brazil, 25–27 m, coll. 1997; UFBA 2859, Recife dos Cascos, Baia de Todos os Santos, Bahia, Brazil, 13–21 m, coll. 2016–2017; MZUSP 2944, CE24, Canal das Arabaianas, Ceará, Brazil.

Description.

Colony encrusting, uni to multilaminar (Fig 12A). Autozooids (Fig 12B) rhombic-polygonal, limited by slightly raised lateral walls, surrounded by a single row of 14–22 marginal pores (0.009–0.019–0.036 mm wide; n = 30; SD = 0.005 mm). Frontal wall rugose and nodular. Primary orifice (Fig 12C) elliptical, wider than long, beaded distal margin with several well-spaced minute denticles, 3–5 oral spines, lyrula narrow, occupying about half of the orifice length (0.020–0.023–0.028 mm wide; n = 10; SD = 0.002 mm), a pair of hooked condyles with coarsely serrated margins. Secondary orifice pear-shaped, forming 2 proximolateral flaps and resulting in a pseudosinus (Fig 12B and 12D), larger in ovicelled zooids (Fig 12D). Adventitious avicularia variable in shapes and sizes (Fig 12A, 12B and 12D), with two morphologies: (1) initially small, narrow and elliptical (Fig 12A), becoming elongate with development (Fig 12B), present at one or both sides below the secondary orifice, proximally oriented, rostrum narrow and slightly curved, slightly corrugated at its lateral margins, rounded tip, palate occupying about half of the rostrum length, oblong foramen and crossbar complete; (2) large lanceolate avicularia with lobate edge at half distal part (Fig 12B and 12D), placed distolaterally to the orifice and oriented proximally, palate broad, occupying about three-quarters of the rostrum length, foramen oval, crossbar complete; 1–2 pseudopores adjacent to the avicularia, rostrum spatulate, with crenulated margins (Fig 12A) in younger and strongly serrated margins (Fig 12B) in older zooids. Ovicells globose (Fig 12D), surrounded by an adjacent frontal wall; ectooecium with 12–27 medium-sized pseudopores (0.005–0.007–0.0013 mm wide; n = 30; SD = 0.001 mm) distributed through the entire ovicell surface. Secondary calcification around the primary orifice in ovicelled zooids forms a hood in the distal margin of the ovicell (Fig 12D).

Remarks.

As like P. ligulata comb. nov., P. serrula belongs to the P. spathulata–P. areolata complex, thus having avicularia with two morphologies: narrow–elongated and large–spatulated. Species of this complex, however, can be distinguished by features of the primary orifice, avicularia ornamentation, and ovicells. Parasmittina serrula differs from P. ligulata comb. nov., P. spathulata, and P. areolata by having up to 6 oral spines (up to 4 in all other species), and large spatulate avicularium with strongly serrated margins (with smoother margins in all other species).

First described based on specimens from Hawaii, in the Central Pacific [2], P. serrula was already recorded from coral reefs of Belize, and experimental panels from Jamaica [3, 37] in the Caribbean and several localities from the Western and Central Pacific [2]. Although most reports of P. serrula from the Western and Central Pacific differ from the type specimens in characters of the primary orifice (Table 7), specimens from SW Atlantic studied here showed all morphological and morphometric characters provided by Soule & Soule [2] (Tables 6 and 7) to P. serrula. Its unusual geographical distribution was already related to hull shipping through the Panama Canal [16] and to an opportunistic behavior of the species [37].

Among congeners, P. serrula is very similar to Parasmittina luteoserrula, recently described by Winston & Jackson [13] based on specimens from the Caribbean. Winston & Jackson [17] compared P. luteoserrula with P. serrula and indicated differences in the zooid sizes (indicated incorrectly as smaller in P. luteoserrula than in P. serrula, but zooids in the former species are actually larger, as shown in Table 6), large avicularia with a more fluted rostrum, and pores occupying more than half of the frontal surface of the ovicell. However, as previously discussed (see remarks of P. alba, for example), much of these variations may be related to different colonial and zooidal stages of development rather than different species. Thus, we consider a species complex involving P. serrula and P. luteoserrula, but additional studies including specimens from the current distributional range of P. serrula are needed.

Distribution.

Central Pacific: Hawaii [3]; SW Atlantic: Brazil (present study).

Material examined.

UFBA 209, 716, 5304, 5313–5315, 5324, 5445, UFPE 831–832, Costa dos Coqueiros, Camaçari, Bahia, Brazil, 25–30 m, coll. 1993–2004; UFBA 365, Salvador, Bahia, Brazil, 0–25 m, coll. 05/04/2012; UFBA 952, 959, 2268, Baia de Todos os Santos, Bahia, Brazil, 0–48 m, coll. 1997–2006; UFBA 3110, 3112, 3116, Costa do Dendê, Bahia, Brazil, coll. 2012; UFBA 5325, Banco Charlotte, Bahia, Brazil, 35 m, coll. 03/1996.

Description.

Colony encrusting, primarily unilaminar (Fig 13A). Autozooids (Fig 13A) initially subrectangular to subquadrangular, limited by slightly raised lateral walls, with a single row of 20–31 marginal pores (0.007–0.019–0.0040 mm in diameter; n = 30; SD = 0.007 mm). Frontal wall rugose and nodular (Fig 13B, 13C). Primary orifice (Fig 13D) elliptical, slightly longer than wide, distal with 4–6 well-spaced minute denticles, up to 3 oral spines, lyrula narrow (0.017–0.031–0.038 mm wide; n = 15; SD = 0.005 mm), a pair of hooked condyles with coarsely serrated margins. Secondary orifice initially developed as two short lateral projections (Fig 13C), sometimes forming a broad U-shaped pseudosinus (Fig 13F). Adventitious avicularia variable in shape and size (Fig 12B–12F), with three morphologies: (1) small, subtriangular, avicularia (Fig 13D), placed laterally at one side of the orifice, distally oriented, rostrum subtriangular, smooth at its lateral margins, pointed tip, palate narrow, subtriangular foramen, and crossbar complete; (2) small, oblong to spatulate avicularia (Fig 13D) single or paired, placed below the secondary orifice, proximally oriented, smooth at its lateral margins, rounded tip, palate occupying about three-quarters of the rostrum length, oval foramen and crossbar complete; (3) large, spatulate avicularia (Fig 13B and 13C), placed laterally at one side of the orifice, oriented proximally, with rostrum oblong to spoon-shaped arched upwards, palate broad occupying three-quarters of the rostrum length, foramen subtriangular to elliptical, with smooth margins and crossbar complete, with 2–3 pseudopores adjacent to the avicularia. Secondary calcification of the frontal wall can place avicularia randomly scattered on the frontal wall (i.e., around the orifice, in a suboral position, and on the ovicell, Fig 13E–13F). Ovicells globose, densely surrounded by adjacent frontal wall (Fig 13E); ectooecium with 8–10 large pseudopores (0.007–0.013–0.026 in diameter; n = 30; SD = 0.004 mm). Secondary calcification around the primary orifice in ovicelled zooids forms a hood in the distal margin of the ovicell (Fig 13F).

Remarks.

Parasmittina simpulata was originally described based on a single infertile colony from southeastern Brazil, being diagnosed by having a primary orifice with distal denticles, serrated condyles, proximolateral small avicularia oval and subtriangular and large avicularia spatulate [12]. All these characters are observed in specimens from coral reefs and experimental plates of tiles from northeastern Brazil analyzed in this study, adding that our colonies have ovicell with large pseudopores (Fig 13E and 13F). Also, we observed that avicularia development and ovicell calcification vary between younger (Fig 13A and 13B) and older (Fig 13C and 13E) colonies.

Parasmittina simpulata is considered very similar to the Caribbean P. barbadensis Winston & Woollacott, 2009 [38], differing only in the large avicularia (absent in P. barbadensis) and larger zooids of P. barbadensis [12]. Unfortunately, P. barbadensis was also described based on a single colony fragment, preventing more comparisons. Parasmittina simpulata and P. barbadensis also share similarities in the frontal calcification, primary and secondary orifices, and avicularia with P. parsevaliformis Soule & Soule, 1973 [2] described based on specimens from Hawaii, except for the large avicularium (absent in P. barbadensis) (Table 8). Soule & Soule [2] described differences in avicularia morphology and secondary calcification in the orifice and ovicell pending the colonial development of P. parsevaliformis. We also found morphological variations in the avicularia development and ovicell calcification when compared younger (Fig 13A and 13B) and older (Fig 13E and 13F) colonies. Also, our values comprise morphometric variations seen in the three taxa–P. simpulata, P. barbadensis and P. parsevaliformis (Table 8). Thus, we have some evidence that the absence of avicularia in specimens originally attributed to P. simpulata and P. barbadensis, respectively, as well as the morphometric variations, can be related to the ontogenetic stage of the studied specimens.

Biogeographically, it is unlikely that P. simpulata (SW Atlantic), P. barbadensis (Caribbean), and P. parsevaliformis (Central Pacific) may represent a single species. On the other hand, P. parsevaliformis was described based on specimens that were encrusting a variety of substrata including rocks, corals, shells and cement [2] and material studied here include colonies from coral reefs and artificial substrata (experimental plates of tiles). Thus, the association with artificial substrata could suggest that a single species of Parasmittina may be dispersing worldwide, resulting in isolated geographical records. However, until more data on these taxa are known, we choose to keep them as distinct species.

Distribution.

SW Atlantic: Brazil [12]; present study).

Material examined.

UFPE 545–554, UFBA 1619, 1621, 1622, 1627, 1628, 1652, 1661, 5319–5322, 5467–5495, Baia de Todos os Santos, Ilha de Itaparica, Itaparica, Bahia, Brazil, intertidal, coll. 2012–2015; UFBA 2852, Baía Todos os Santos, Porto da Barra, Salvador, Bahia, Brazil, 24 m, coll. 07/2017, UFBA 575, 2847–2849, Costa dos Coqueiros, Camaçari, Bahia, Brazil, 22–27 m, coll. 1997–2002, UFBA 697, 5003, Costa do Dendê, Bahia, Brazil, 30 m, coll. 2002; UFPE 641–644, UFBA 5316, Praia do Francês, Marechal Deodoro, Alagoas, Brazil, coll. 03/02/2003; UFPE 651, Jatiuca, Maceio, Alagoas, Brazil, coll. 15/10/2005; MZUSP Uncatalogued PE26, UFPE 579, Porto de Suape, Cabo de Santo Agostinho, Pernambuco, Brazil, coll. 01/08/2020; UFPE 621, 649 Barra de Catuama, Goiana, Pernambuco, Brazil; UFBA 5323, Pontas de Pedra, Goiana, Pernambuco, Brazil, intertidal, coll. 20/02/2015, UFPE 343, 645–646, Porto do Cabedelo, Cabedelo, Paraíba, Brazil, intertidal, coll. 27/09/2009; UFPE 274, Saco da Pedra, coll. 16/09/2004; UFPE 340, Amores, 22/09/2006; UFBA 5017, 5160, 5167, 5212, 5262, 5276, 5293, 5405, 5421, 5459, 5496, 5499, 5511, 5513, Baia de Todos os Santos, Salvador, Bahia, Brazil, 3–5 m, coll. 2012, MZUSP 887, Santos, São Paulo, Brazil.

Description.

Colony encrusting, unilaminar. Autozooids (Fig 14A) subrectangular to polygonal, limited by slightly raised lateral walls, with a single row of 25–30 large marginal pores (0.009–0.025–0.042 mm in diameter; n = 30; SD = 0.008 mm). Frontal wall slightly rugose and nodular. Primary orifice (Fig 14B) elliptical, slightly longer than wide, anter smooth, 1–2 oral spines, lyrula narrow (0.020–0.041 mm wide), and a pair of hook-shaped condyles with coarsely serrated tips. Secondary orifice low (Fig 14D), forming two lateral short projections. Adventitious avicularia variable in shapes and sizes (Fig 14B and 14F), with three morphologies: (1) small, subtriangular avicularia (Fig 14C and 14D), placed laterally to the orifice and distally oriented in autozooids, with a suboral or randomly arranged in ovicelled and adjacent zooids (Fig 14E–14F), rostrum subtriangular, smooth at its lateral margins, pointed tip, palate narrow, elliptical foramen and crossbar complete; (2) small, spatulate avicularia (Fig 14B and 14C), placed o zooidal margins, commonly replacing a marginal pore; (3) large, spatulate avicularia (Fig 14B and 14C), placed laterally at one side of the orifice, oriented distally, palate broad occupying half of the rostrum length, foramen subtriangular to elliptical, with smooth margins and crossbar complete, with 2–3 pseudopores adjacent to the avicularia. Ovicell (Fig 14E–14F) densely surrounded by adjacent frontal wall, soon becoming immersed in the frontal calcification; ectooecium with 20–32 medium-sized pseudopores (0.004–0.016 mm in diameter).

Remarks.

Almeida et al. [58] redescribed P. loxoides based on specimens from Brazil. They characterized it by having subrectangular to polygonal autozooids with large marginal pores (Fig 14A), 1–2 oral spines (Fig 14B and 14D), narrow and short lyrula, condyles with serrated margins, and large avicularia distally directed. However, all these characteristics are also seen in P. winstonae, first described based on specimens from China by Liu et al. [45]. Moreover, no morphometric differences were seen among specimens from Brazil and China (Table 9) (see also Tilbrook [8, 57]. Thus, here we consider P. winstonae as the senior synonym of P. loxoides.

Among all congeners, P. winstonae most resembles P. californica (Robertson, 1908), P. collifera (Robertson, 1908) and P. regularis Soule & Soule, 2002 in having three types of avicularia–lateral, marginal, and large distally directed. However, whereas the large avicularium of P. winstonae is spatulate with a rounded tip, that of P. californica, P. collifera and P. regularis is subtriangular with an acute rostrum.

Like other species described here, P. winstonae haves an unusual geographic distribution in the Western and Central Pacific and SW Atlantic [8, 12, 45, 57, 58]. Interestingly, Chinese and Brazilian specimens of P. winstonae showed a common association with bivalve shells of the genus Pinctada Röding, 1798 [45, 58]. Colonies from Brazil studied here are also from artificial substrata, and specimens from Malaysia studied by Taylor & Tan [57] were encrusting shells on a rope hanging from a jetty. Therefore, passive dispersal may be related to the current distributional range of P. winstonae.

Distribution.

Western and Central Pacific: China, Islands Solomon and Malaysia [8, 45, 57]; SW Atlantic: Brazil [12, 58] present study.

Material examined.

Holotype: UFBA 714, Camaçari, Bahia, Brazil, 50 m, coll. 07/2004. Paratypes: UFBA 314, Costa do Descobrimento, Banco Charlotte, Bahia, Brazil, 35 m coll. 03/1996; UFBA 953, Baía de Todos os Santos, Bahia, Brazil, coll. 27/05/1997; UFBA 948, Baía de Todos os Santos, Bahia, Brazil, coll. 29/05/1997. Additional specimens: UFBA 5000, Banco Besnard, Espírito Santo, Brazil, coll. 04/1996; UFPE 3100–3101, Ilhas Rasas, Guarapari, Espírito Santo, Brazil, 11–15 m, coll. 27/03/2017; UFPE 3102–3105, Ilha Escalvada, Guarapari, Espírito Santo, Brazil, 15m, coll. 29/03/2017. UFPE 2599.1, Fortaleza, Ceara, Brazil, 24-27m. Coll. 1965–1966.

Etymology.

Alluding to the profile of the large avicularium, subspatulate to sublanceolate, that leaves a falciform (hooked) outline.

Diagnosis.

Parasmittina with elliptical orifice, smooth distal margin, lyrula occupying three quarters of the orifice width, and robust downward-facing condyles with serrated margin. Secondary orifice low, forming side flaps without hiding the lyrula. Adventitious avicularia subtriangular smaller and large subspatulate to sublanceolate, with hooked tip, placed distolaterally to the orifice and with rostrum oriented proximolaterally. Ovicell globose with 20–32 medium-sized pseudopores distributed through the entire ovicell surface.

Description.

Colony encrusting, uni to multilaminar. Autozooids (0.322–0.432–0.584 mm length; n = 15; SD = 0.075 mm; 0.270–0.369–0.460 mm wide; n = 15; SD = 0.063 mm), (Fig 15A and 15B) subrectangular to subquadrangular, limited by slightly raised lateral walls, surrounded by a single row of 14–24 marginal pores (0.011–0.025–0.052 mm in diameter; n = 30; SD = 0.010 mm). Frontal wall with several rounded nodules (Fig 15A and 15B). Primary orifice (0.062–0.081–0.0.94 mm length; n = 15; SD = 0.009 mm; 0.087–0.098–0.105 mm wide; n = 15; SD = 0.004), (Fig 15D) elliptical, longer than wide, distal margin smooth, 1–2 oral spines, lyrula large (0.049–0.058–0.076 mm wide; n = 15; SD = 0.006 mm), comprising half of the orificial width, a pair of hooked condyles with serrated margins. Secondary orifice forming 2 proximolateral flaps resulting in a pseudosinus (Fig 15B and 15D), larger in ovicelled zooids (Fig 15E). Adventitious avicularia variable in shape and size (Fig 15B), with two morphologies: (1) small to moderate in size (0.154–0.169–0.184 mm in length; n = 3; SD = 0.014 mm; 0.052–0.064–0.078 mm in wide; n = 3; SD = 0.013 mm), subtriangular avicularia (Fig 15B), with a hooked tip and large foramen, placed distolaterally to the orifice, with rostrum oriented proximolaterally; (2) large avicularia (Fig 15B and 15C) (0.336–0.384–0.457 mm in length; n = 9; SD = 0.039mm; 0.077–0.083–0.088 mm in wide; n = 9; SD = 0.004 mm), reaching almost the entire zooidal length, profile subspatulate to sublanceolate, broad palate, occupying about half rostrum, foramen elliptical, rostrum subtriangular, with smooth margins, hooked tip and crossbar complete; 3–6 pseudopores adjacent to the avicularia, placed distolaterally to the orifice with rostrum oriented proximally. Ovicells (Fig 15E and 15F) (0.156–0.176–0.212 mm in length; n = 15; SD = 0.016mm; 0.153–0.198–0.240 mm in wide; n = 15; SD = 0.021 mm) globose, densely surrounded by adjacent frontal wall (Fig 15F); ectooecium with 25–30 medium-sized pseudopores (0.003–0.007–0.012 in diameter; n = 30; SD = 0.002 mm) distributed through the entire ovicell surface.

Remarks.

Specimens of P. falciformis sp. nov. were previously attributed to P. munita by Almeida et al. [26] that is known from Australia [48]. However, it is distinguished from P. falciformis sp. nov. by the number of spines (3 in P. munita and up to 2 in P. falciformis sp. nov.) shape of pseudosinus (deep in P. munita and shallow in P. falciformis sp. nov.) and profile of the small adventitious avicularia (oblong in P. munita and subtriangular in P. falciformis sp. nov.).

Other specimens of Parasmittina from Brazil were also attributed to Smittina trispinosa var. munita [23, 33]. Although these specimens have avicularia similar to that of P. falciformis sp. nov., differences among these taxa include the number of oral spines (3 in specimens from Marcus and 2 in P. falciformis sp. nov.), secondary orifice (shorter in P. falciformis sp. nov.), pseudosinus (shallower in P. falciformis), and rostrum of the small adventitious avicularia (straight in specimens from Marcus and curved in P. falciformis sp. nov.). Moreover, specimens studied by Marcus [23, 34] have also a large interzooidal avicularia, not observed in P. falciformis sp. nov. Thus, here we consider that Smittina trispinosa var. munita described by Marcus [23, 34] represent a distinct taxon than P. munita and P. facilformis sp. nov.

The combination of primary orifice with large lyrula, smooth distally, 1–2 oral spines, serrated condyles with hooked tips, and two types of avicularia distinguishes P. falciformis sp. nov. from all congeners.

Distribution.

SW Atlantic: Brazil (present study).