Septibranchia (Mollusca: Bivalvia) from the North and Northeast Coasts of Brazil

Septibranchia comprises groups of bivalves that have developed a series of anatomical and conchological modifications toward a carnivorous and/or saprophagic lifestyle. The present study aims to identify the species of the families Poromyidae, Cuspidariidae and Verticordiidae found off the northern and north-eastern coasts of Brazil, reducing the gaps in the geographic distribution and adding new morphological data of the analysed shells. Six genera and eight species were found in the 54 examined lots: Cardiomya cleryana, Cardiomya ornatissima, Cardiomya perrostrata, Cuspidaria sp., Plectodon braziliensis, Myonera aff. paucistriata, Poromya cf. granulata and Trigonulina ornata. The present study adds new conchological and morphometric characteristics to descriptions of species, redulces the gap in the distribution of Plectodon braziliensis in the Southwestern Atlantic, and extends the northern distribution limit of P. braziliensis and C. cleryana with new records for off the north-north-east coast of Brazil. By adding new morphological and morphometric data of the shells, the present study may help in the taxonomy of these septibranch species. New collections in the region will probably lead to the discovery of new records of Septibranchia.


Background
Anomalodesmata Dall, 1889, which diversified early in the Palaeozoic, is a monophyletic clade, globally distributed and represented today by a diverse assemblage of highly specialised marine shallow and deep waters bivalves (Harper et al. 2006;Bieler et al. 2014). Several families of anomalodesmatans have become carnivorous, showing a series of remarkable anatomical and conchological modifications for the capture of small arthropods and polychaetes (Harper et al. 2006;Morton 1981). This main group of carnivorous taxa has been grouped together as the 'septibranchs' (Harper et al. 2006). Some analyses of molecular and/or morphological data support a deep division of Anomalodesmata into three clades: Septibranchia and two lineages corresponding to the 'lyonsiid' and largely to the 'thraciid' lineages (Harper et al. 2006;Bieler et al. 2014). However, the origin of the carnivorous septibranch mode of life remains unresolved, due to conflicting results from different analyses (Bieler et al. 2014). This study will discuss three families within Anomalodesmata: Poromyidae Dall, 1886, Cuspidariidae Dall, 1886, and Verticordiidae Stoliczka, 1870 Poromyidae is characterized by a small, fragile, inflated, and usually equivalve shell, with a rounded anterior end and a truncate posterior end; it is sculptured with radial striae or granulates (Olsson 1961;Abbott 1974;Coan et al. 2000). Species of this family have exhalant siphon short and inhalant siphon eversible into large raptorial hoods; their gills are absent and they are simultaneously hermaphroditic (Abbott 1974;Coan et al. 2000). Poromyidae, known from Cretaceous, is widely distributed in deep water, where they are shallowly infaunal in fine sediments (Olsson 1961;Abbott 1974).
Cuspidariidae species are mostly inhabitants of deep water, occurring between 4 and 6,800 m depth (Abbott 1974;Coan et al. 2000;Coan and Valentich-Scott 2012). Cuspidariids have separate sexes and are carnivores or detritus consumers. Their shell is generally small, thin, inflated, and inequilateral, with a rounded and convex anterior end and rostrate or pointed posterior end (drawn out into the tubular rostrum in many) (Olsson 1961;Abbott 1974;Coan et al. 2000).
Verticordiidae, known from the early Cretaceous, contains highly modified genera, mostly deep-water infauna capturing and feeding on small invertebrates (Coan et al. 2000). The shell is generally small, cardiform, equivalve, inequilateral, and inflated; radial sculpture is usually present, often of riblets or lirae; the surface is often granular or spinose (Olsson 1961;Coan et al. 2000).
According to Rios (2009) and Oliveira (2012), 37 species are recorded in these families in Brazil: two genus and three species in Poromyidae, seven genus and 26 species in Cuspidariidae, and five genus and eight species in Verticordiidae. Studies on the north-north-east coast of Brazil are still scarce, with a majority of studies focusing on the south-eastern region (Oliveira 2012;Oliveira and Absalão 2007, 2010a, 2010bSimone and Cunha 2008;Absalão and Oliveira 2011 (Rios 2009) recorded Cardiomya ornatissima (d'Orbigny, 1853) and Cardiomya perrostrata (Dall, 1881) in Brazilian waters, but did not specify the localities.
The present study aims to identify the species of the families Poromyidae, Cuspidariidae and Verticordiidae found in the northern and north-eastern coasts of Brazil, reducing the gaps in the geographic distribution and adding new morphological data for the analysed shells.

Identification key
The dichotomous identification key proposal to identify the eight studied species is below.  (Rios 2009;Janssen and Krylova 2014).
In the present study, this species was recorded for off the coast of Pará (north Brazil).
Remarks: This material was allocated in the genus Poromya because it has an external surface sculptured with fine granules and right valve with a strong cardinal tooth in front of a chondrophore. Other four living genera are recognized in Poromyidae: Cetomya Dall, 1889 (weak cardinal tooth in right valve), Dermatomya Dall, 1889 (smooth outer surface), Lissomya Krylova, 1997 (smooth outer surface), and Dilemma Leal, 2008 (shell strongly compressed in the anteroposterior direction) (Coan et al. 2000;Krylova 1997;Leal 1764). According to Rios (2009) and Oliveira (2012), two species are recorded granulata has both ends rounded and a greater number of minute granules in the external surface, whereas P. cymata has a posterior end with a narrow, radial keel (Rios 2009). The examined material in this study has both ends rounded and an external surface with numerous granules, just like P. granulata sensu Rios (2009), but is distinguished from the latter mainly by the non-elongated posterior end. This difference may be due to the fact that our material is of young specimens. Thus, we prefer to identify it as Poromya cf. granulata.
According to Bieler et al. (2010), two families are recorded in superfamily Poromyoidea: Poromyidae and Cetoconchidae Ridewood, 1903, and one genera is recognized in Cetoconchidae: Cetoconcha Dall, 1886. Cetoconcha differs from Poromya mainly by "the dentition obsolete except the cardinal tooth of the right valve, which itself is sometimes absent in the adult, though observable in the young shells" (p. 280) (Dall 1886). Our specimens could be juveniles of Cetoconcha. However, our material differs from the descriptions of species of Cetoconcha (e.g., Cetoconcha bulla (Dall, 1881) and Cetoconcha braziliensis Allen & Morgan, 1981), especially regarding ornamentation present in the outer surface. Cetoconcha bulla has a "shell smooth, except that a faint impression of radiating lines is left by the epidermis" (p. 107) (Dall 1881), while C. braziliensis has a "shell surface with faint, concentric growth lines, about 13 posterior radial lines of granules, more distinct ventrally" (p. 521) (Allen and Morgan 1981). Thus, we decided to keep our material in genus Poromya. Unfortunately, it was not possible to identify more accurately the specimens due to the existence of only two young right valves.
Geographic distribution: Atlantic Ocean: off the coast of Pará (north Brazil) Bathymetric distribution: 77 m deep Remarks: This material was allocated in the genus Cuspidaria Nardo, 1840 because it has a smooth external surface with fine growth lines, without granules. Absalão and Oliveira (2011) carried out a revision of the species of Cuspidaria present on the continental slope (700-2,000 m) of the Campos Basin (22°S) off southeastern Brazil, describing two new species. According to Oliveira (2012), 11 species are recorded in genus Cuspidaria in Brazil: Cuspidaria rostrata (Spengler, 1793), C. circinata (Jeffreys, 1876), C. papyria (Jeffreys, 1876), C. platensis (Smith, 1885), C. wollastonii (Smith, 1885), Cuspidaria? monosteira Dall, 1890, C. parva Verrill & Bush, 1898, Cuspidaria cf. barnardi Knudsen, 1970, C. krylovae Allen, 2011, C. tamandua Oliveira, 2011, andC. wapixana Absalão &Oliveira, 2011. The material examined in this study does not appear to belong to any known species of Cuspidaria. Unfortunately, it was not possible to identify the specimen at a specific level due to its poor preservation and the existence of a single left valve.
Genus  angled on either side of beaks, anterior straight at first, then curving into the rounded end. Rostrum rounded posteriorly. Color white, inner surface shiny (polished). Inequilateral, posterior end longer, umbones slightly opisthogyrate. Outer surface with fine growth lines and dense minute granules. Hinge in the right valve with elongate (lamellar) lateral teeth (anterior and posterior). Hinge in the left valve without teeth, with small fossete.
Geographic distribution: Atlantic Ocean: Brazil (Ceará, Rio de Janeiro, Santa Catarina and Rio Grande do Sul) (Rios 2009;Pimpão et al. 2010). In the present study, this species was recorded for off the north-north-east coast of Brazil (Amapá, Pará, Ceará, Alagoas, and Bahia).
Remarks: Plectodon braziliensis was formerly placed in the genus Cuspidaria, but Pimpão et al. (2010) reallocated it in genus Plectodon because it has minute granules upon the external surface. According to these authors, Plectodon braziliensis is the only species of this genus recorded from Brazil. Plectodon braziliensis is distinguished from P. scaber (from the Pacific Ocean) mainly by a rose-tinged umbo (Pimpão et al. 2010). This study reduces the gap in the distribution of P. braziliensis in the South-western Atlantic and extends the northern distribution limit with new records for off the northnorth-east coast of Brazil (Amapá, Pará, Alagoas, and Bahia). Now the Amapá coast is its most northern limit.
Genus Description: Shell ovate (11.4 × 6.9 mm), inequilateral, longer anteriorly, valves inflated, posteriorly rostrate. Rostrum sometimes with fine radial lines. Color white. Umbones opisthogyrate. Sculptured with variable number (15-36) curved radial ribs, that extend beyond the shell edge, yielding a crenulated margin. Ribs concentrated in the anterior region, with distance between them increasing from anterior to posterior. Hinge in the right valve with strong posterior lateral tooth, small fossete. Hinge in the left valve without teeth, with fossete.
Geographic distribution: Atlantic Ocean: Rio de Janeiro, Brazil, to Tierra del Fuego and Falkland Island, Argentina (Rios 2009). In the present study, this species was recorded for off the north-north-east coast Brazil (Amapá, Pará, and Alagoas) and Itamaracá Island, Pernambuco (northeast Brazil).    (Dall, 1881), and Cardiomya striata (Jeffreys, 1876). Cardiomya cleryana is distinguished from other Cardiomya species found in this study mainly by radial ribs with equal sizes and shortly rostrate posteriorly. The anatomy of the arenophilic system of Cardiomya cleryana was described by Oliveira and Sartori (2014). This study extends the northern distribution limit of C. cleryana in the South-western Atlantic with new records for off the north-north-east coast of Brazil (Amapá, Pará, and Alagoas) and Itamaracá Island, Pernambuco (northeast Brazil). Now off the Amapá coast is its northernmost limit.
Cardiomya ornatissima (  with thin light-brown periostracum. Subequilateral, posterior end longer, umbones slightly opisthogyrate. Right valve convex, with 6-11 prominent radial ribs with interspaces, broader in the posterior region, that extend beyond the edge, making the crenulated margin, ribs well marked on the inner surface of the valve; rostrum truncate, with fine secondary ribs (1-3) and growth lines; hinge with l elongate (lamellar) lateral tooth (posterior), anterior region rounded wih projetion next to umbones, deep fossete. Left valve very convex, with 7-16 prominent radial ribs with interspaces, broader in the posterior region, that extend beyond the edge, making the crenulated margin, ribs well marked on the inner surface of the valve; rostrum median truncate, with fine secondary ribs (3-6) and growth lines; hinge without teeth, with deep fossete.
Geographic distribution: Atlantic Ocean: North Carolina to Yucatan, Caribbean and Brazil (Rios 2009;Correa-Sandoval and Rodríguez-Castro 2013). In the present study, this species was recorded for off the north-northeast coast of Brazil (Amapá, Pará, Ceará, and Alagoas).
Remarks: Cardiomya ornatissima is distinguished from other Cardiomya species found in this study mainly by a smaller number of radial ribs that are well-marked on the inner surface of the valve and the presence of secondary ribs in the rostrum.
Cardiomya perrostrata (Dall, 1881) (Figs. 1 and 7, Table 4)  (7) Description: Shell small (14.93 × 9.45 mm), with a long, narrow rostrum (sometimes with fine lines). Color white, inner surface shiny. Subequilateral, posterior end longer, umbones opisthogyrate. Sculptured with 14 to 32 radial ribs alternating in size, every other one being slightly larger than the other, stronger in the posterior region. Growth lines well marked in some specimens. Crenulated margin. Hinge in the right valve with posterior lateral teeth, with small fossete. Hinge in the left valve without teeth.
Geographic distribution: Atlantic Ocean: North Carolina to Florida, Caribbean, Brazil (Rios 2009;Correa-Sandoval and Rodríguez-Castro 2013). In the present study, this species was recorded for off the north-northeast coast of Brazil (Amapá, Ceará, and Alagoas) and Itamaracá Island, Pernambuco (northeast Brazil).
Habitat: Muddy sand bottoms (Rios 2009). Remarks: Cardiomya perrostrata is distinguished from  Description: Valve small (5.01 × 3.08 mm), ovate, shortly rostrate (1 mm in lenght), with 2 strong keels posteriorly (3 ribs well marked and one secondary rib). Outer surface white and shiny. Inequilateral, umbones opisthogyrate. Sculptured with radial and concentric lines that ceases just before the anterior keel. The space between and behind kells is smooth. Left valve without teeth.
Geographic distribution: Indian Ocean: west coast of Malabar (Allen and Morgan 1981); Pacific Ocean (Janssen and Krylova 2014); Atlantic Ocean: North Carolina to Caribbean, Brazil (Campos Basin, Rio de Janeiro) (Rios 2009;Oliveira and Absalão 2009 (Oliveira and Absalão 2009). The examined material in this study is shortly rostrate, with two strong keels posteriorly just like Myonera paucistriata, but is distinguished from the latter mainly by its radial and concentric lines and a well-marked third rib. Unfortunately, it was not possible to identify the specimens at a specific level due to the existence of a single left valve.
Superfamily Description: Shell small (5.6 × 5.9 mm), equivalve, ovate to rounded, compressed. Color white to cream, inner surface silver-white, outer surface opaque (not shiny). Umbones subcentral, turned to the anterior region; deep lunule. Ligament long. Outer surface with minute granules. 3/ 4 of the anterior surface of the valve sculptured with 10 to 13 curved, deep radial ribs. Posterior region without lines. Anteroventral margin crenulated by the strong ribs. Hinge in the right valve with small cardinal teeth, below umbones. Hinge in the left valve without teeth.
Habitat: Muddy and sand bottoms and clays (Rios 1994;Lamy et al. 2014). Remarks: Trigonulina ornata was formerly placed in the genus Verticordia J. de C. Sowerby, 1844, but the new combination was proposed by Poutiers and Bernard (1995), based on the presence of a series of prominent radial ribs and the crenulation of the posteroventral margin. According to Oliveira (2012), Trigonulina ornata is the only species of this genus recorded from Brazil. Trigonulina ornata has a large distribution in the western Atlantic, and it had previously been recorded off the coast of Amapá (north Brazil) (Rios 1994).

Discussion
Although several studies have been carried out in Brazil with the families Poromyidae, Cuspidariidae, and Verticordiidae in the last few years (e.g. (Oliveira 2012;Oliveira and Absalão 2009, 2010a, 2010bAbsalão and Oliveira 2011;Pimpão et al. 2010;Oliveira and Sartori 2014)) the knowledge about these families is still far from complete, as shown by the new records done in this study. The present study shows the possibility of two new species of septibranchs to Brazil. However, it was not possible to reach conclusive identifications due to the scarce materials (one valve of each species) and its poor preservation. Oliveira (2012) points out that one of the main issues regarding Septibranchia is disordered creation of new taxa with the analysis of a few characters, which is not uncommon to exhibit great phenotypic plasticity. Most descriptions of the species discussed here do not distinguish between right and left valves, nor do they provide a more detailed study of morphometry and relevant characters in the differentiation within and between species. By adding new morphological and some morphometric data of the shells, the present study may help in the taxonomy of the septibranchs species. Unfortunately, the amount of morphometric data obtained in this study did not allow their use for distinguishing among analysed species (few shells and many of them poorly preserved). However, we believe that these data are important and may help future morphometric studies.

Conclusion
This study provide new knowledge about Septibranchia on the Brazilian coast, reducing the gaps in the geographic distribution and extending the distribution limits of some species with new records. New collections probably will discover new records of Poromyidae, Cuspidariidae, and Verticordiidae in the region.