An illustrated checklist of macrofaunal molluscs from softsediments of the Abrolhos Parcel (northeastern, Brazil) with 15 new records*

Flávia Maria Pereira da COSTA , Ana Maria Setubal PIRES-VANIN

Departamento de Oceanografia Biológica, Instituto Oceanográfico, Universidade de São Paulo, São Paulo 05508-120, Brazil

Abstract Comprehensive understanding of marine biodiversity is essential for conservation, especially for vulnerable ecosystems. In this paper, we implemented and illustrated a checklist of molluscs from the Abrolhos Parcel, Brazil, the most important coralline area in South Atlantic waters. The list features 100 species belonging to 4 classes and 85 genera, of which 15 are new records for Bahia State, northeast Brazil.The results highlight the potential for new records in the area. The species came from 54 unconsolidated sediment samples collected from the bottom of the reef with a 0.042-m2 van Veen grab. Among the listed species, Curveulima sp., Notarchus sp. and Guyanella clenchi are new records for the South Atlantic, while Caecum metamorphosicum, Eratoidea janeiroensis, Volvarina serrei, Solemya notialis, Solariorbis shimeri,and Amphithalamus glabrus are endemic to Brazilian waters. A comparison of our results with those obtained in other reef environments indicates that the Abrolhos Parcel has a rich malacofauna and suggests that many more species can still be found with more samplings.

Keyword: Bivalvia; Gastropoda; micromolluscs; Scaphopoda; Solenogastres; southwest Atlantic

1 INTRODUCTION

Mollusca is one of the most specious animal groups on Earth, being surpassed only by the arthropods. In marine environments, the diversity of mollusc species(c. 52 000) is comparable to arthropods (c. 55 000 species), making up 25% of all species reported for the marine benthos (Bouchet, 2006; Appeltans et al.,2012). Mollusc diversity is also notable high in tropical waters, particularly in reef areas (Bouchet et al., 2002).

Mollusc inventories have often been conducted in diff erent marine ecosystems (Kantor and Sysoev,2005). In Brazil, with the exception of some pioneering work (e.g., Morretes, 1949; Rios 1970,1985), mollusc diversity remains poorly known in many regions, and marine micromolluscs (i.e.,specimens smaller than 10 mm) are especially neglected (Bouchet et al., 2002; Absalão, 2005).These small organisms require specific procedures to collect and classify, and the taxonomy of many species is very problematic (Bouchet et al., 2002).Most of studies are focused on coastal areas due to easier access and lower costs compared to the open sea. Consequently, many of these areas need to be researched to better understand their faunas. This knowledge has proved fundamental for ecological studies in view of the growing interest in biodiversity datasets for conservation and management purposes.Accordingly, preliminary species list are fundamental for environmental studies at large (Bouchet, 1997;Gofas et al., 2017).

The invertebrate fauna of the Abrolhos Reef Bank is largely unknown, despite the biological importance of the area, which houses the massive coral reef formation in the South Atlantic. Due to the ecological significance of molluscs and the area itself the present study grows in relevance.

Fig.1 Abrolhos Bank in eastern Brazilian Continental Shelf and sampling sites in the Abrolhos Parcel

Table 1 Coordinates and depth of the nine areas sampled in the Abrolhos Parcel

2 MATERIAL AND METHOD

Specimens were collected during the Benthos Subproject within the PROABROLHOS Project(Productivity and Sustainability of the Abrolhos Bank) with the objective of studying the distribution and structure of benthic fauna in coral reefs of the Abrolhos Bank, Eastern Brazilian Continental Shelf.

Abrolhos Bank (16°40′S-19°40′S and 37°20′W-39°10′W) is the largest extension of the Eastern Brazilian Continental Shelf, reaching up to 200 km in length. It encompasses the largest known reef complex in the South Atlantic and covers about 46 000 km2, of which about 18% is occupied by coral reefs (Melo et al., 1975; Muehe, 1987). The site is recognized unique because it has a large number of sediments—increasing the water turbidity in some areas, mushroom-shaped reef structures, and a high degree of endemism of coral species (Leão, 1999;Leão et al., 2003; Dutra et al., 2005). The study site is located in the Abrolhos Parcel at the Abrolhos Bank,a large system of submerged reefs within the Abrolhos Marine National Park, created in 1983. It extends from north to southeast of the Abrolhos Archipelago and marks the transition between siliciclastic and carbonatic sediments.

Nine sites were sampled in uncompacted sediments in two campaigns (July 2007 and January 2008) in the Abrolhos Parcel (Fig.1; Table 1) with a 0.042-m2van Veen grab in triplicate. The retrieved sediments were sieved through a 500-μm mesh and preserved in 70%ethanol. In the laboratory, molluscs were identified based on Rios (1985, 2009); Warén (1980, 1983) for Eulimidae; Lima and Christoff ersen (2016) and Lima et al. (2013) for Caecidae; and Silva-Filho et al.(2012) for Scaphopoda. Only samples with soft parts were analyzed in order to avoid mixing species from distant locations carried by the surrounding water currents. Scientific names were updated after the World Register of Marine Species taxonomic database(WoRMS Editorial Board, 2018), and the main shell measurements were taken from digital photographs using the ImageJ software (Rasband and Image,1997-2018). Specimens are deposited in the Museu de Zoologia (MZSP) and Coleção Biológica Prof.Edmundo F. Nonato, both from the University of São Paulo, and part in the Museu Nacional do Rio de Janeiro (MNRJ).

3 RESULT AND DISCUSSION

We identified 100 species belonging to 85 genera and 59 families (Table 2). Although most of the diversity of marine molluscs comprises gastropods(Appeltans et al., 2012), we found a similar number of bivalve species in the present samples. Gastropoda comprised 31 families and 42 genera, while Bivalvia was represented by 26 families and 40 genera (Figs.2& 3). Of the 100 species recorded, 50 were gastropods,46 bivalves, 3 scaphopods and 1 solenogastres. In addition, many recorded taxa are probably part of complexes of species that still need revision, such as Gibberula lavalleeana, Lapinura divae and Atys sp.In some cases, juvenile specimens were classified above the species level, mainly at the genus level, and listed as “sp.” like the Thyasira, Okenia, and Galeommatoidea, and await further studies.

Although the sampling method employed here is most suitable for collecting endofaunistic organisms,we found a significant number of epifaunal species,such as Crenella decussata, Lioberus castanea,Musculus lateralis, Pinctada imbricata, Cyclopecten sp., Similipecten sp., Chama sp., Euvola ziczac,Limaria pellucida, Calyptraea centralis, Conus sp.,Aplysia parvula and Solenogastres, as well as parasitic groups such as Curveulima sp., Eulimastoma sp.,Eulimostraca sp., Melanella sp., and Turbonilla sp.

The species reported here represent almost 6% of all marine mollusc diversity recorded for Brazil according to Rios (2009). The present paper adds 48 species to the previous list by Absalão (2005) of the Abrolhos Bank, which highlights the relevance of the present samples.

Lamellaria branca Simone, 2004 is currently recorded in Uruguay and São Paulo State, Brazil,from 58-134 m depth, and the Brazilian endemic species Amphithalamus glabrus Simone, 1996 has been found in shallow waters (5 m) off São Paulo State (23°S). The geographic distribution of both species is extended herein north to Abrolhos, Bahia State (17°58′S), and their bathymetric range is expanded to 18 and 16.5 m, respectively. Similarly,Amalda josecarlosi, Diplodonta punctata, Solariorbis shimeri, Temnoconcha galathaea, Transennella cubaniana, Eratoidea janeiroensis, Nuculana concentrica, and Solemya notialis are firstly reported to Bahia State, but their depth ranges remain the same.Notarchus, of which two species are known from the Mediterranean and the Indo-Pacific, and Curveulima,recorded for northern Atlantic and Indo-Pacific, are herein recorded for the first time in Brazil. Moreover,two additional species have their distribution extended to Abrolhos: Guyanella clenchi, previously reported from the Caribbean Sea, and Okenia impexa from São Paulo State. Furthermore, some other species had their geographic and bathymetric ranges addressed,such as Nucinella serrei and Similipecten sp., usually reported in deeper waters (Taylor and Glover, 2010).

Table 2 Mollusc species and the respective number ofindividuals recorded for the Abrolhos Parcel during the PROABROLHOS surveys

Table 2 Continued

Table 2 Continued

Fig.2 Gastropod specimens sampled in soft sediment at Abrolhos Parcel (NE Brazil)

Fig.2 Continued

Fig.3 Bivalvia, Scaphopoda, and Solenogastres sampled in soft sediment at Abrolhos Parcel (NE Brazil)

Fig.3 Continued

The largest number of specimens was grouped in Caecidae and Semelidae, with six and four species,respectively. Despite the overall high number of species registered in the area, only seven were found in all sites. In terms of abundance, Caecum brasilicum,Caecum floridanum, Crenella decussata, and Solenogastres sp. represented over 50% of the specimens. The genus Caecum Fleming, 1813 was widely distributed in the area and is the largest group with 634 specimens, with the minute Caecum floridanum Stimpson, 1851 as the most abundant species (20.7% of all molluscs sampled). This occurrence was probably related to the ability of this species to exploit a large number of habitats. Caecum species are typically associated with mangrove roots,rocks, limestone substrates, and sediment grains adjacent to the reefs (Abbott, 1974; Mello and Maestrati, 1986; Pizzini et al., 1998).

The presence of the bivalve families Lucinidae (5 spp.), Thyasiridae (2 spp.) and Solemyidae (1 sp.) in the Abrolhos Parcel is remarkable. Species of thesefamilies often live in organically enriched environments such as mangroves, dense algal beds(Glover et al., 2008) and sewage disposal sites (Reid and Brand, 1986) associated with chemosynthetic bacteria (Dame, 1996). In Lucinidae, the most diverse group of symbiotic molluscs, the endosymbiotic relationship with sulphide-oxidizing or even methaneoxidizing bacteria is mandatory (Taylor and Glover,2016; Mikkelsen and Bieler, 2008). Although already addressed to oligotrophic environments (Glover and Taylor, 2007), the presence of these species in poorlyknown areas reinforces the relevance ofinventory studies. This is especially true when these areas are compared to other heavily sample reef environments,such as those of the Indo-West Pacific, which are known to have Lucinidae as one of the most abundant bivalve families (Bouchet et al., 2002).

Table 3 Comparison among mollusc richness in uncompacted sediments from the Abrolhos Parcel and other reefs around the world

The present work also contributed to the expansion of the geographical distribution of Solemya notialis Simone, 2009 and Guyanella clenchi Altena, 1968,both species previously known to have very restricted distributions. The first one is described to Southern Brazil and the second was previously reported to the Caribbean Sea (Taylor and Glover, 2016).

Regarding the relatively small area and narrow bathymetric range accessed, the high number of reported species suggests that much more can be found with a significant intensification of sampling.However, we assume that species richness continually increases with increasing sediment volume, but, as this may not be entirely true, this value may be overestimated. Table 3 lists the species richness data obtained from other papers dealing with the number of mollusc species in areas elsewhere. The sample eff ort of each data was transformed to cubic meters(m3) to allow comparisons. Our results indicate a significant number of species for the Abrolhos Parcel,about 5 times higher than that reported for the 23-mile Reefin North Carolina (Posey and Ambrose, 1994).In fact, the number of species is astonishing in the Abrolhos Bank as a whole. Despite the raw number reported by Absalão (2005) for Abrolhos Bank being almost thrice that from our results, we found a similar number of species when considering only the Abrolhos Parcel. The small discrepancy in numbers that favors the results of Absalão may be related to the origin of the material, as the author examined live specimens and empty shells in his study. Moreover,considering the similar research discussed, the list presented here shows an important and rich malacofauna living in the unconsolidated sediments around the Abrolhos reefs.

4 CONCLUSION

One hundred species were identified in the unconsolidated sediment of the Abrolhos Parcel. The high number of species in a relatively small area suggests that the Abrolhos Parcel sustains a high diversity of molluscs, superior to other previously studied reef areas. The well-preserved specimens allowed us to extend the distribution range of 15 species. Some of them were previously recognized only for their empty shells, which are not always a good element to consider in ecological studies. The high number of samples with soft parts found in this study may support future approaches in studies on Mollusca.

5 DATA AVAILABILITY STATEMENT

The data that support the findings are all presented herein.

6 ACKNOWLEDGMENT

The authors express their gratitude to the following taxonomists that helped in identifying several species:Sergio A. Vanin (Instituto de Biociências da Universidade de São Paulo, IBUSP), Luiz Simone(Museu de Zoologia da Universidade de São Paulo,MZSP), Carlo Magenta (Universidade Metropolitana de Santos, UNIMES), Silvio Lima (Universidade Federal de Campina Grande, UFCG), Alexandre Pimenta (Museu Nacional do Rio de Janeiro, MNRJ),Leonardo Souza (MNRJ), and Bárbara Valentas-Romera (MZSP). This work was conducted as part of the multidisciplinary project “Produtividade,Sustentabilidade e Utilização do Banco de Abrolhos”,Subproject Benthos, supported by “Conselho Nacional de Desenvolvimento Científico e Tecnológico”- CNPq - given to AMSP-V (proc.#420219/2005-6) and in part by the MSc fellowship from CNPq given to FMPC (proc. #130159/2016-6).The materials were collected under the permit number 722773 from IBAMA, Brazilian Ministry of Environment, to Eurico C. Oliveira Filho of the University of São Paulo.