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Research Article
A new species of Cellaria (Bryozoa: Cheilostomata) from northeastern Brazil, with a tabular identification key to the Atlantic species
expand article infoAna C.S. Almeida, Facelúcia B.C. Souza§, Leandro M. Vieira
‡ Universidade Federal de Pernambuco, Recife, Brazil
§ Universidade Federal da Bahia, Salvador, Brazil
Open Access

Abstract

A new species of the erect cheilostome bryozoan Cellaria Ellis & Solander, 1786 is described from Bahia, NE Brazil. Cellaria oraneae sp. nov. is the first formally characterized species of the genus reported from Northeastern coast of Brazil, distinguished from all congeners by the combination of hexagonal autozooids and rhomboid fertile zooids, hexagonal interzooidal avicularium with sagittate foramen, completely immersed ovicell with oval aperture and proximal rectangular lip. A brief discussion of the diversity of Cellaria from the Atlantic Ocean and a tabular identification key to these species are also provided.

Key words

Bryozoan, Cellariidae, taxonomy, Western Atlantic

Introduction

Marine bryozoans are found in all oceans, from the intertidal to abyssal depths. The vast majority of some 5,689 living species (Bock and Gordon 2013) belongs to Order Cheilostomata Busk, 1852, which shows a wide variety of colonial growth forms, from encrusting laminar to erect colonies (Taylor and James 2013). Encrusting colonies seem to be more abundant in tropical regions, whereas erect bryozoans are particularly diverse in temperate and polar waters. (Barnes and Whittington 1999, Taylor and James 2013).

Among the erect bryozoans, Cellaria Ellis & Solander, 1786 is a speciose genus, comprising more than 50 living species (Hayward and Thorpe 1989, Bock and Hayward 2014). Colonies have articulated skeletal elements (internodes) joined by chitinous joints, with each internode containing multiple zooids (Taylor and James 2013). Cellaria species may occur from less than 20 to over 1000 m deep in all oceans. They are common in shallow, coastal waters, attached to hard substrata (McKinney and Jaklin 2000, 2001, Hayward and McKinney 2002). Most Cellaria are known from the Indo-Pacific regions, Antarctica and Northeast Atlantic, being apparently limited to their expected native distribution (Hayward and Thorpe 1989). Only a few species have been documented from the Western Atlantic (Winston and Woollacott 2009, Bock and Hayward 2014). However, in the past few years, five new species were described from this region – Cellaria brasiliensis Winston, Vieira & Woollacott, 2014, Cellaria riograndensis Ramalho & Calliari, 2015 and Cellaria subtropicalis Vieira, Gordon, Souza & Haddad, 2010 from Brazil; Cellaria novanglia Winston & Hayward, 2012 and Cellaria louisorum Winston & Woollacott, 2009 from United States and Barbados, respectively. This indicates that the diversity of Cellaria from the Atlantic is yet to be described.

Over the past decade, knowledge of the diversity of marine bryozoans in Brazil has grown significantly and more than 100 new species were described (e.g., Vieira et al. 2010, 2012, 2014, Winston and Vieira 2013, Winston et al. 2014, Almeida et al. 2015a, Ramalho and Calliari 2015). Although Cellaria have been documented in the Brazilian waters since the 1960s (Braga 1967, Vieira et al. 2008), the first species from Brazil, C. subtropicalis, was only recently formally characterized and described (Vieira et al. 2010). Since then, two other new species were described, C. brasiliensis from Rio de Janeiro (Winston et al. 2014), and C. riograndensis, from Rio Grande do Sul (Ramalho and Calliari 2015). These three valid species from the Brazilian coast are from South and Southeastern Brazil, and there is a record of a new species from Bahia (Vieira et al. 2008, Almeida et al. 2015b). This species was named Cellaria bahiensis in a doctoral dissertation but never formally described (Vieira et al. 2008). Therefore, according to the International Code of Zoological Nomenclature Article 9.7 and Article 11.1 (ICZN 1999), the name Cellaria bahiensis Souza is a nomen nudum and cannot be considered valid, as pointed by Vieira et al. (2008).

Here we formally describe this new taxon from state of Bahia, Northeast Brazil, and provide a diagnosis for it based on specimens from the same locality (i.e. Todos os Santos Bay) as those studied by Souza (Vieira et al. 2008).

Material and methods

All type and non-type specimens analyzed in this study are deposited in the Museu de Zoologia of Universidade Federal da Bahia (UFBA), Salvador, Brazil. The specimens were collected by dredge in different localities between 1997 and 2006 along the coast of Bahia, northeast Brazil, from 15 to 50 m (Fig. 1). Some specimens were collected by Laboratório de Malacologia e Ecologia de Bentos (LAMEB) from Universidade Federal da Bahia (UFBA) on different years but at the same locality, and were deposited in a single lot for each locality. Selected specimens were coated with gold-palladium alloy and examined under a scanning electron microscopy (JEOL JSM-6390LV) at Centro de Pesquisa Gonçalo Moniz (FIOCRUZ/BA), Bahia, Brazil. Measurements were taken from digital SEM images of the holotype using ImageJ® software, including range (minimum and maximum), mean, and standard deviation.

Figure 1. 

Distribution map of Cellaria oraneae sp. nov. in state of Bahia, northeast Brazil. (BA) Bahia, (CA) Camaçari, (SSA) Salvador, (TSB) Todos os Santos Bay, (BS) Baixo Sul, (AB) Abrolhos Bank.

Taxonomy

Order Cheilostomata Busk, 1852

Suborder Neocheilostomina d’Hondt, 1985

Cellariidae Fleming, 1828

Cellaria Ellis & Solander, 1786

Cellaria oraneae sp. nov.

Figs 2–7

Cellaria sp. 2: Vieira et al. 2008: 21. [Brazil: Bahia]

Cellaria sp.: Almeida et al. 2015a: 4. [Brazil: Bahia]

Diagnosis

Cellaria with hexagonal autozooids, opesia semi-elliptical with distal rim tuberculate and slightly convex proximal rim with two rounded condyles; interzooidal avicularia hexagonal, with longitudinal ridges forming a spear-shaped area, with sagittate foramen and placed only between non-fertile zooids; fertile zooids rhomboid and ovicell completely immersed with oval aperture and a proximal rectangular lip.

Description

Colony erect, cylindrical, jointed, symmetrically bifurcating and attached at the base by chitinous rhizoids. Branches formed by 6–20 zooidal series, 0.353–0.372 mm in diameter when formed only by infertile autozooids, but larger in regions of fertile zooids, about 0.544–0.574 mm in diameter (Fig. 2). Autozooids hexagonal in outline, about 0.358–0.409 mm (0.395 ± 0.016) long and 0.164–0.231 mm (0.211 ± 0.019) wide, limited by raised lateral walls, comprising a pair of longitudinal ridges extending from lateral walls forming a somewhat lanceolate area (Fig. 3). Frontal wall with a sunken granular cryptocyst. Opesia semi-elliptical, about 0.056–0.068 mm (0.62 ± 0.003) long and 0.072–0.095 mm (0.085 ± 0.006) wide, distal rim tuberculate and arched, proximal rim smooth and slightly convex, two rounded denticles placed near proximal corners (Fig. 4). Interzooidal avicularium sometimes present, about 0.340–0.367 mm (0.354 ± 0.010) long and 0.186–0.210 mm (0.198 ± 0.009) wide, with same cryptocystal calcification and longitudinal ridges as autozooids, forming a spear-shaped area; foramen sagittate, tapered distal edge, convex proximally, forming a broad lip, placed only between infertile zooids (Fig. 5). Fertile zooids wider than autozooids, rhomboid in outline, about 0.316–0.374 mm (0.355 ± 0.016) long and 0.200–0.320 mm (0.285 ± 0.038) wide; opesia semi-elliptical, about 0.050–0.069 mm (0.60 ± 0.004) long and 0.078–0.115 mm (0.103 ± 0.009) wide, same cryptocystal calcification and longitudinal ridges as autozooids (Fig. 6). Ovicells completely immersed, aperture oval with a proximal rectangular lip (Fig. 7).

Material examined

Holotype: Brazil, Bahia: Todos os Santos Bay (12°51’62”S, 38°39’78”W, 43 m), 1 specimen, April 1997, Orane Alves leg., UFBA 280. Paratypes: Brazil, Bahia: Todos os Santos Bay (12°49’62”S, 38°37’38”W), 1 specimen, May 1997, Orane Alves leg., UFBA 2263; Salvador (12°58’79”S, 38°33’41”W, 50 m), 1 specimen, UFBA 2262. Additional specimens: Brazil, Bahia: Abrolhos Bank (18°20’80”S, 38°55’97”W, 41 m), 10 specimens, April 1997, Zelinda Leão leg., UFBA 1446; Maraú (Baixo Sul, 14°06’49”S, 38°57’31”W), 5 specimens, August 2004, LAMEB-UFBA leg., UFBA 2261; Cairú (Baixo Sul, 13°27’01”S, 38°46’34”W, 48 m), 2 specimens, 2002, José Dominguez leg., UFBA 2260; Ituberá (Baixo Sul, 13°44’02”S, 38°48’58”W, 47 m), 6 specimens, 2002, José Dominguez leg., UFBA 2259; Maraú (Baixo Sul, 14°05’00”S, 38°53’55”W, 30 m), 6 specimens, 2002, José Dominguez leg., UFBA 2258; Itacaré (Baixo Sul, 14°11’01”S, 38°58’59”W, 15 m), 8 specimens, 2002, José Dominguez leg., UFBA 2241; Camaçari (12°44’12”S, 38°05’12”W, 23 m), 4 specimens, 2002-2004, LAMEB-UFBA leg., UFBA 2257; Camaçari (12°50’00”S, 38°10’06”W, 37 m), 6 specimens, 2002-2006, LAMEB-UFBA leg., UFBA 2256.

Distribution

Atlantic: Brazil (Bahia); infralittoral, from 15 to 50 m.

Etymology

The species epithet is in honor of Orane Alves (Universidade Federal da Bahia), in recognition of her contribution to the knowledge of Brazil’s marine biodiversity.

Remarks

Cellaria oraneae sp. nov. can be distinguished from all congeners by the combination of hexagonal autozooids and rhomboid fertile zooids, hexagonal interzooidal avicularia with longitudinal ridges forming a spear-shaped area and with sagittate foramen, ovicell completely immersed with aperture oval and a proximal rectangular lip. We analyzed 50 internodes of the new species, among which 30 were formed only by autozooids (infertile internodes) and 20 were fertile (with autozooids and ovicelled zooids). Avicularia were found in both fertile and infertile internodes, but no avicularia were found between fertile zooids. Therefore, we believe that interzooidal avicularia of C. oraneae sp. nov. are placed only between autozooids.

Among Cellaria species already recorded from the Atlantic Ocean, C. oraneae sp. nov. resembles C. riograndensis in having cryptocyst mostly granular, hexagonal interzooidal avicularia with longitudinal ridges forming a spear-shaped area, with no condyles and completely immersed ovicell. Cellaria oraneae sp. nov. can be distinguished from C. riograndensis by having autozooids hexagonal and fertile rhomboid zooids (in C. riograndensis, both autozooids and fertile zooids have the same shape), avicularia placed only between autozooids and with sagittate foramen (avicularia is placed between either autozooids and fertile zooids and with triangular foramen in C. riograndensis), and ovicell aperture with a proximal rectangular lip (without lip in C. riograndensis).

Among other Cellaria distributed worldwide, C. oranae sp. nov. resembles C. tenuirostris (Busk, 1852) in the hexagonal autozooids and rhomboid fertile zooids, granular cryptocyst, hexagonal interzooidal avicularia with longitudinal ridges forming a spear-shaped area and completely immersed ovicell. Cellaria oranae sp. nov. is distinct from C. tenuirostris, however, by having avicularium with sagittate foramen and no condyles (C. tenuirostris have an avicularium with triangular foramen and well-developed condyles), avicularium placed only between autozooids (in C. tenuirostris avicularia are placed between either autozooids and fertile zooids), and ovicell aperture with a proximal rectangular lip (without lip in C. tenuirostris).

Figures 2–7. 

Cellaria oraneae sp. nov., UFBA 280, holotype, Bahia, Brazil: (2) general aspect of the branches; (3) close-up of subhexagonal autozooids; (4) close-up of opesia showing tuberculate distal rim and proximal condyles; (5) close-up of hexagonal interzooidal avicularia with longitudinal ridges forming a spear-shaped area and sagittate foramen; (6) close-up of fertile rhombic zooids; (7) close-up of immersed ovicells showing oval aperture with proximal rectangular lip. Scale bars: 2 = 500 µm; 3, 6 = 200 µm; 4, 5, 7 = 100 µm.

Discussion

The morphological characters commonly used to discriminate among Cellaria species include the shape of autozooids and fertile zooids (assigned as hexagonal when formed by six sides or rhomboid when with four sides; Hastings 1947), opesial condyles, type of avicularia and shape of its foramen, ovicell and its aperture. Species of Cellaria show a wide range of morphologies, which include species with condyles at the distal opesial rim or at both distal and proximal opesial rim; avicularium large, interzooidal (i.e. replacing one autozooid; Hayward and Ryland 1998) or small, fistulose-like (i.e. interposed in the longitudinal series of autozooids; Hayward and Ryland 1998 and Berning 2013); and ovicells slightly prominent or completely immersed, with aperture varying from a single entire fenestra or ornamented with a proximal lip. The foramen of the avicularia, either interzooidal or fistulose, shows several morphologies, including bell-shaped (i.e. forming an inverted U-shaped curve; López de La Cuadra and García-Gómez 1996); triangular (i.e. three sides with pointed tips); subtriangular (i.e. three sides with rounded edges); semicircular (i.e. as long as wide); semielliptical (i.e. longer than wide); subcordate (i.e. somewhat heart-shaped; López de La Cuadra and García-Gómez 1996); mushroom-shaped (i.e. resembling the profile of a mushroom; Winston and Hayward 2012) and sagittate (i.e. shaped like an arrowhead, Table 1). As known in other bryozoan genera (e.g., Vieira et al. 2013, Almeida et al. 2014), the analysis and characterization the morphology of the ovicell/ooecia are needed to make a taxonomic assignment. In the absence of fertile colonies, it is difficult to assign specimens to any known species using only autozooidal characteristics.

At least 58 species of Cellaria are recognized worldwide (Bock and Hayward 2014). So far, 23 species have been recorded from the Atlantic Ocean and, among these, 12 from the Western Atlantic. Cellaria oraneae n. sp. is the fourth species of the genus described from Brazil, representing the only species from the Northeast. Since there are few studies on the continental shelf and slope of the Brazilian Northeast, where the genus seems to be common, it is likely that the diversity of Cellaria from Brazil has been underestimated. This seems to be the case with other Brazilian bryozoan taxa (e.g., Vieira et al. 2010, Almeida and Souza 2014, Winston et al. 2014, Almeida et al. 2014, 2015a). The real diversity of the genus around the world is also difficult to estimate, since many records have been attributed to the widely-known C. tenuirostris, restricted to the Indo-Pacific Oceans (Hastings 1947, Winston 2005). Additionally, some species assigned to Cellaria are only known from their original descriptions (e.g., Cellaria ornata d’Orbigny, 1842, Cellaria triangulata Canu & Bassler, 1925). Without more recent morphological characterization or comparison with related taxa, the validity of some of these may be questionable. Comprehensive studies using SEM are still lacking, preventing the elucidation of the identity of some species as Cellaria clavata (Busk, 1884), Cellaria salicornia (Pallas, 1766) and Cellaria normani (Hastings, 1947) (Hastings 1947, Hayward and Thorpe 1989, López de La Cuadra and García-Gómez 1996). As pointed out by Cook (1967), a review of these taxa is recommended.

Tabular identification key to Atlantic species of Cellaria: present (+) and absent (–), avicularia interzooidal (I), avicularia fistulose (F), unknown states (?).

Species Autozooid Opesia Avicularia Dimorphism in fertile zooid Ovicell/Aperture
Shape Cryptocyst Distal rim Proximal rim Distal condyles Type Shape Foramen Condyles
C. atlantida Cook, 1967 rhombic granular beaded convex I rhombic bell-shaped immersed/with rectangular lip
C. bassleri Hastings, 1947 rhombic smooth smooth convex I hexagonal subtriangular immersed/semicircular
C. bafouri Matsuyama, Titschack, Baum & Freiwald, 2015 hexagonal smooth beaded convex immersed/with rectangular lip
C. brasiliensis Winston, Vieira & Woollacott, 2014 hexagonal granular beaded convex I hexagonal subtriangular + immersed/oval to circular
C. clavata (Busk, 1884) rhombic granular beaded convex + F semicircular semicircular + (hexagonal) immersed/circular, with rectangular lip in later astogeny
C. cookae Lopez de la Cuadra & García-Gómez, 1996 hexagonal granular beaded convex I hexagonal subcordate immersed/with rectangular lip
C. crassa Wood, 1844 hexagonal granular ? convex + I rhombic subtriangular + (rhombic) immersed/semicircular
C. diffusa Robertson, 1905 hexagonal granular beaded convex + F quadrangular semicircular immersed/oval
C. elongatoides Bassler, 1936 hexagonal granular ? convex F circular semicircular + (with larger opesial condyles) immersed/with semicircular lip
C. fistulosa (Linnaeus, 1758) rhombic/hexagonal granular beaded convex F quadrangular to rounded semielliptical + immersed/circular, with rectangular lip in later astogeny
C. harmelini d’Hondt, 1973 hexagonal smooth beaded convex F semicircular semicircular - immersed/with rectangular lip
C. louisorum Winston & Woollacott, 2009 hexagonal granular beaded convex I hexagonal triangular + + (with concave proximal rim) immersed/circular
C. normani (Hastings, 1947) hexagonal granular beaded convex I hexagonal semicircular + immersed/oval to circular
C. novanglia Winston & Hayward, 2012 hexagonal granular beaded convex F quadrangular mushroom-shaped + immersed/with rectangular lip
C. oraneae sp. hexagonal granular beaded convex I hexagonal sagittate + (rhombic) immersed/with rectangular lip
C. ornata d’Orbigny, 1842
rhombic granular beaded convex ? I ? triangular ? ? ?
C. paradoxa Hayward & Cook, 1979 hexagonal granular smooth convex + + (rhombic, with larger opesia) immersed/semicircular
C. riograndensis Ramalho & Calliari, 2015 rhombic/hexagonal granular beaded convex I hexagonal triangular immersed/circular
C. salicornioides Lamouroux, 1816 hexagonal granular beaded convex + I hexagonal semicircular + immersed/circular
C. scoresbyi Hastings, 1947 hexagonal granular beaded convex - I hexagonal triangular + immersed/with rectangular lip
C. sinuosa (Hassall, 1840) hexagonal granular smooth straight + F circular semicircular + immersed/with rectangular lip
C. sobrionoi Lopez de la Cuadra & García-Gómez, 2000 hexagonal granular beaded convex I rhombic subtriangular + prominent/triangular
C. subtropicalis Vieira, Gordon, Souza & Haddad, 2010 rhombic/hexagonal granular beaded convex I hexagonal subtriangular + Immersed/semielliptical to subtriangular
C. triangulata Canu & Bassler, 1925 rhombic smooth ? straight ? ? ? ? + (with larger opesia) immersed/triangular

Acknowledgments

This study is part of A.C.S. Almeida’s PhD thesis supported by PROTAX-CNPq (440620/2015-5) through the Graduate Program in Animal Biology (Programa de Pós-Graduação em Biologia Animal) of the Departamento de Zoologia, UFPE. We are grateful to Centro de Pesquisa Gonçalo Moniz (FIOCRUZ/BA) for SEM images, Orane Alves (Laboratório de Geoecologia de Sedimentos Marinhos, UFBA), Marlene Peso-Aguiar (Laboratório de Malacologia e Ecologia de Bentos, UFBA) and Ulisses Pinheiro (Laboratório de Porifera, UFPE) for logistical support.

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