Nassarius foveolatus (Gastropoda, Nassariidae), a new record of an exotic species in Brazil

Abstract

Exotic species are those that occur in an area beyond their natural limit and they are considered invasive when they cause harm to the economy, environment, or human health. In coastal environments, ballast water and inlays on the hull and other parts of vessels are the main ways of introducing invasive aquatic alien species. Nassarius foveolatus (Dunker, 1847) is native from the Central and East Indian Ocean to the East China Sea. The first specimens (empty shells) of N. foveolatus were collected manually on November 11, 2017 on the Rocio footbridge, located in the Paranaguá Estuarine Complex, on the coast of the State of Paraná, southern Brazil. Posteriorly, live specimens were collected in other localities of this bay. It is already possible to infer that the specimens of N. foveolatus occur together with the native specimens of N. vibex (Say, 1822), having the same niche. As previously only N. vibex existed in that place, at least a displacement of this native species has been occurred. However, certainly future ecological studies may confirm this displacement and additional consequences to the local ecosystem, as nassariids can be predators and scavengers. Control procedures should be also greatly implemented.

Key-Words
Invasive; Exotic; Mollusca; Nassarius foveolatus; Paraná coast

INTRODUCTION

Exotic, non-native or introduced species are those that occur in an area beyond their natural limit and they are considered invasive when they cause harm to the economy, environment, or human health (Carlton, 1996). Bioinvasions, i.e., the introduction of alien species into different ecosystems, are the major causes of biodiversity loss in the world, causing damage to local species and to the functioning of ecosystems (Stachowicz et al., 1999; Silva & Barros, 2011).

In coastal environments, ballast water (with sediments) and inlays on the hull and other parts of vessels are the main ways of introducing invasive aquatic alien species (Ferreira et al., 2004). Ballast water introduces aquatic organisms that are harmful to the environmental balance (including bacteria and viruses), both in marine and freshwater ecosystems, degrading important commercial activities such as those associated with fishing (Souza et al., 2009).

Nassariidae is a family of almost exclusively marine detritivores snails inhabiting bottoms of unconsolidated substrates and, to a lesser extent, rocky shores in tropical waters, with greater abundance between 0 and 300 m deep (Nekhaev, 2014). This group belongs to the neogastropod superfamily Buccinoidea and consists of more than 400 species (Brown, 1982; Galindo et al., 2016) divided into 18 extant genera, of which Buccinanops d’Orbigny, 1841 and Nassarius Duméril, 1805, are the largest genera in the family currently represented in the Brazilian coast (Rios, 2009; Rosenberg, 2009). In Brazilian waters, nine species of Nassarius have been recorded (Abbate & Cavallari, 2013).

The typical shells of the family Nassariidae are characterized as being small to medium, with short and curved siphonal canal, conical protoconch, and horny operculum (Rios, 2009). It presents a high shell spire, oval shape with or without shoulder in the opening. The surface of the shell may be smooth or may exhibit axial and spiral sculptures (Abbate & Cavallari, 2013; Rios, 2009). Most nassariids have a well-developed callus. It has a rich fossil record dated since the Late Cretaceous (Taylor et al., 1980; Van Dingenen et al., 2015; Galindo et al., 2016).

The genus Nassarius and its close relatives tend to be restricted to muddy environments, though a few species shelter among loose rocks and sand. Ecologically, most species of Nassarius are thought to be facultative scavengers inhabiting inter- to subtidal shallow marine environments. As scavengers, they are important in maintaining the balance of ecological systems, especially for the benthic community (Cernohorsky, 1984). Their taxonomy, especially the status of the alleged genera and subgenera, is still far from a resolution and the distribution of most species is poorly understood (Cavallari & Abbate, 2013; Galindo et al., 2016). Compared to other gastropods, Nassarius snails have a relatively long planktonic larval phase, leading to a high level of dispersal capacity by marine currents (Tallmark, 1980). They can also be transported by ballast water and oysters farming to other environments and, by surviving, consequently becoming exotic species (e.g.,Carlton, 1992; Bachelet et al., 2004; Townsend et al., 2010; Fofonoff et al., 2018; Goka, 2019).

Nassarius foveolatus (Dunker, 1847) is native from Central and East Indian Ocean to East China Sea, including countries as Mauritius, Pakistan, India, Myanmar, Thailand, Singapore, Malaysia and China (Cernohorsky, 1984; Subba Rao et al., 1992; Raut et al., 2005; Rosenberg, 2006; Robba et al., 2007; Tan & Woo, 2010; Zhang & Yang, 2010; Mahapatro et al., 2018). It presents a small, oval, slightly striated shell with furrowed suture, columella with slight callosity, denticulate external lip, and long and narrow feet.

The aim of this study is to report the first occurrence of the exotic species N. foveolatus in Brazil, confirmed both by morphological and molecular approaches. A discussion on its possible via of transportation and environmental consequences is also included.

MATERIAL AND METHODS

The first specimens (empty shells) of an unknown Nassarius species were collected manually on November 11, 2017, on the Rocio footbridge (25°30.236′S 48°31.891′W), located in the Paranaguá Estuarine Complex, on the coast of the state of Paraná, southern Brazil (Fig. 1). Subsequently, on December 17, 2017, live specimens were collected in the same locality. The material collected was deposited in the molluscan collections of the Museu de Zoologia da Universidade de São Paulo, São Paulo, Brazil (MZUSP 136955, 3 spm.; MZUSP 143545, 11 spm.; MZUSP 143546, 20 spm.; MZUSP 143617, 14 spm.; MZUSP 143618, 16 spm.) and at the Laboratório de Ecologia Aplicada e Bioinvasões, Pontal do Paraná, Brazil (LEBIO 577, 9 spm.; LEBIO 578, 6 spm.).

Figure 1
Paranaguá Estuarine Complex and sites where Nassarius foveolatus was found. Black square = Port of Paranaguá; 1 = Ponta da Pita; 2 = Europinha; 3 = Lamin Island; 4 = Rocio; 5 = Emboguaçu River.

The morphological identification was done according to Cernohorsky (1984). To confirm the morphological identification, molecular identification was performed using the DNA Barcode method (Hebert et al., 2003). Firstly, the genomic DNA was extracted using the EZ-DNA kit (Biological Industries) from muscle. Then, a fragment of 650 bp of the cytochrome oxidase subunit 1 (COI) was sequenced. The amplification comprises a PCR with 25 ul final concentrations of 2.5x buffer, 3 mM of MgCl2, 0.4 uM of dNTP, 0.1 pmol of each HCO and LCO (Folmer et al., 1994), 0.1 U of Taq Polymerase and 50 ng of DNA template. PCR product was purified using PEG 8000 (Amresco Inc., Cleveland, OH, USA). The sequencing reactions were performed with BigDye® kit (Applied Biosystems) according the manufacturer protocol and was purified with Sephadex G-50 (GE Healthcare Bio-Sciences AB, Uppsala, Sweden). The final product was sequenced in an ABI 3130 Genetic Analyzer (Applied Biosystems).

The identification was confirmed though Neighbor-Joining (NJ) and Bayesian (BI) trees. Sequences of Nassarius spp. accessed from GenBank (see species and accession number in Table 1) were used as reference sequences and Antillophos sp. (GU393391.1) was used as outgroup. Sequences were aligned using the Muscle Algorithm (Edgar, 2004) in Geneious 2019.1.1. The NJ was constructed in Geneious, using the Tamura-Nei evolution model (Tamura & Nei, 1993) and 10 thousand bootstraps. The BI tree was constructed in the Beast 1.8 (Drummond et al., 2012), with three independent runs of 100 million MCMC generations sampled each 10,000 trees, 10% of burn-in and substitution model indicated by jModeltest 2.1.10 (Darriba et al., 2012).

Table 1
Species of Nassarius accessed from GenBank and accession numbers.

Species	Accession number	Species	Accession number	Species	Accession number
Antillophossp.	GU393391.1	Nassarius foveolatus	NC041546.1	Nassarius olivaceus	KY451342.1
Nassarius acuminatus	GU393380.1	Nassarius fraterculus	KX069667.1	Nassarius olivaceus	MG682443.1
Nassarius acuminatus	KY100533.1	Nassarius fraudulentus	KY451303.1	Nassarius olomea	KY451343.1
Nassarius acuminatus	KY451253.1	Nassarius fretorum	KY451304.1	Nassarius oneratus	KY451344.1
Nassarius acuticostus	KY100534.1	Nassarius gaudiosus	KY451305.1	Nassarius pagodus	FM999173.1
Nassarius acuticostus	KY451254.1	Nassarius glans	KT754006.1	Nassarius papillosus	KY451347.1
Nassarius agapetus	KY451255.1	Nassarius glans	KY451308.1	Nassarius persicus	LC167813.1
Nassarius albescens	KY499727.1	Nassarius globosus	KY451306.1	Nassarius poupini	KY451351.1
Nassarius algidus	KY100535.1	Nassarius globosus	KY451309.1	Nassarius pullus	JQ975555.1
Nassarius algidus	KY100536.1	Nassarius graniferus	KY451311.1	Nassarius pullus	KY100627.1
Nassarius algidus	GU393388.1	Nassarius haldemani	KY451313.1	Nassarius pullus	KY451353.1
Nassarius algidus	GU393389.1	Nassarius hepaticus	JQ975462.1	Nassarius radians	KC970054.1
Nassarius arcularia	KY451259.1	Nassarius hepaticus	FJ660667.1	Nassarius radians	KC970058.1
Nassarius arcularia	KY451340.1	Nassarius hepaticus	FJ660644.1	Nassarius reeveanus	KY451355.1
Nassarius arcus	KY451260.1	Nassarius herosae	KY451314.1	Nassarius reticulatus	EF571446.1
Nassarius babylonicus	KY451261.1	Nassarius hirasei	KY100588.1	Nassarius reticulatus	KR084688.1
Nassarius barsdelli	KY451262.1	Nassarius hirasei	KY100589.1	Nassarius rufus	KY451358.1
Nassarius bellulus	KY451263.1	Nassarius horridus	KY451240.1	Nassarius samiae	KY451359.1
Nassarius bicallosus	KY451264.1	Nassarius houbricki	KC970035.1	Nassarius semiplicatus	JQ975563.1
Nassarius bimaculosus	KY451265.1	Nassarius houbricki	KC970031.1	Nassarius semiplicatus	JQ975564.1
Nassarius boucheti	KY451266.1	Nassarius idyllius	KY451345.1	Nassarius semisulcatus	KY451360.1
Nassarius callospira	KY451267.1	Nassarius incrassatus	KT988325.1	Nassarius sinarus	KX519508.1
Nassarius camelus	KY451268.1	Nassarius incrassatus	KU714729.1	Nassarius sinarus	KY100645.1
Nassarius cinctellus	KY451279.1	Nassarius incrassatus	MG934953.1	Nassarius sinusigerus	KY451363.1
Nassarius cinnamomeus	KY451280.1	Nassarius interliratus	KY451316.1	Nassarius siquijorensis	JQ975552.1
Nassarius concinnus	KY451283.1	Nassarius irus	KY451317.1	Nassarius siquijorensis	KP253020.1
Nassarius concinnus	KY451364.1	Nassarius javanus	KY451318.1	Nassarius splendidulus	KY451365.1
Nassarius conoidalis	JQ975565.1	Nassarius kooli	KY451321.1	Nassarius stigmarius	KY451392.1
Nassarius conoidalis	KY451284.1	Nassarius kraussianus	EF636006.1	Nassarius subspinosus	KY451243.1
Nassarius coronatus	KY451287.1	Nassarius kraussianus	KY451322.1	Nassarius subtranslucidus	KY451393.1
Nassarius crematus	KY451288.1	Nassarius labordei	KY451323.1	Nassarius succinctus	KP253021.1
Nassarius crematus	KY451330.1	Nassarius leptospirus	KY451324.1	Nassarius succinctus	JQ975500.1
Nassarius crenoliratus	KY451289.1	Nassarius limnaeiformis	KY451325.1	Nassarius succinctus	JQ975501.1
Nassarius cuvierii	JQ950234.1	Nassarius livescens	JQ975514.1	Nassarius succinctus	KY100688.1
Nassarius dijki	KY451293.1	Nassarius livescens	KY100592.1	Nassarius sufflatus	KT290129.1
Nassarius disparilis	KY451294.1	Nassarius lochi	KY451326.1	Nassarius sufflatus	GU393387.1
Nassarius distortus	KY451295.1	Nassarius luridus	KY451327.1	Nassarius sufflatus	KY100689.1
Nassarius dorsatus	JQ975553.1	Nassarius margaritifer	KY451329.1	Nassarius sufflatus	KY100691.1
Nassarius dorsatus	JQ975554.1	Nassarius martinezi	KC970050.1	Nassarius sufflatus	KY100694.1
Nassarius dorsuosus	KY451296.1	Nassarius mendicus	KX069671.1	Nassarius tabescens	KY451394.1
Nassarius ecstilbus	KY451297.1	Nassarius moolenbeeki	KY451332.1	Nassarius teretiusculus	KY100695.1
Nassarius euglyptus	KX519509.1	Nassarius multicostatus	KY451333.1	Nassarius thachi	KX519507.1
Nassarius euglyptus	KY100558.1	Nassarius multipunctatus	KY451334.1	Nassarius thachi	KY451395.1
Nassarius euglyptus	KY451299.1	Nassarius nigrus	KY451241.1	Nassarius vanpeli	KY451399.1
Nassarius eximius	KY451300.1	Nassarius nitidus	GU270625.1	Nassarius vanuatuensis	KC970062.1
Nassarius fenistratus	KY451301.1	Nassarius nitidus	MG934857.1	Nassarius velvetosus	KC970064.1
Nassarius festivus	JQ975431.1	Nassarius nodifer	KY100593.1	Nassarius velvetosus	KC970063.1
Nassarius festivus	AB642676.1	Nassarius nodifer	KY100621.1	Nassarius venustus	KY451400.1
Nassarius filosus	KY451302.1	Nassarius noguchii	KY451338.1	Nassarius vibex	KU905981.1
Nassarius foveolatus	KY100587.1	Nassarius novaezelandiae	KY451339.1	Nassarius vitiensis	KY451403.1
Nassarius foveolatus	MH346209.1	Nassarius ocellatus	KY451341.1

RESULTS AND DISCUSSION

As referred above, the specimens of N. foveolatus (Fig. 2A-B) were initially collected in Rocio, Paranaguá, Paraná. This locality is adjacent to Dom Pedro II Port (Port of Paranaguá), one of the largest in Brazil, which suggests that the species may have been introduced through ballast water. On the site, there is a small patch of mangrove bordered by a tidal flat with marshes. During low tides the plain is exposed, keeping some pools of water. Inside and around these pools, active live specimens were found at densities of up to 11 individuals/m², in sympatry with N. vibex (Say, 1822) (Fig. 2C-D). The native N. vibex can be easily distinguished by being smaller, with the peristome callus much more developed in the adult specimens, by the thicker outer lip, and by the spire sculpture of strong axial ribs.

Figure 2
Shells of Nassarius found in Paranaguá Estuarine Complex. H: Shell height; D: shell greatest diameter. (A) Ventral view of N. foveolatus; (B) Dorsal view of N. foveolatus; (A-B) LEBIO 577 #2; H = 17.2 mm; D = 9.4 mm. (C) Ventral view of N. vibex; (D) Dorsal view of N. vibex; (C-D) LEBIO 347; H = 18.6 mm; D = 14.7 mm.

For the Bay of Bengal, in Odisha state, India, Ghosh et al. (2017) found a density of up to 11.8 individuals/m² of N. foveolatus, suggesting that the density of this species in the Paranaguá Estuarine Complex is already reaching the same levels as those observed in its natural environment. On June 5, 2019, living individuals of N. foveolatus were found in the Emboguaçu River, in the Lamin Island, in Europinha (Vista Bela), and also in Ponta da Pita, all localities in the Paranaguá Estuarine Complex (Fig. 1).

The genetic identification for N. foveolatus suggested both by NJ (Fig. 3A) and BI (Fig. 3B) trees is highly supported. Interestingly, a sequence deposited as N. hepaticus (Pulteney, 1799) (FJ660644.1) in GenBank was also assigned to this group. However, since the other sequences of this species were assigned in a distant clade with N. nodifer (Powys, 1835) (see Appendices session for the entire phylogeny), this sequence probably represents an error of identification (as both species have similar shells) or even introgression between N. hepaticus and N. foveolatus, process already proposed for other Nassarius species (for details, see Pu et al., 2017).

Figure 3
Summarized genetic identification of the focal individual through (A) Neighbor-Joining and (B) Bayesian trees of the COI fragment. Only bootstrap values higher than 70% (A) and posterior probabilities higher than 0.70 (B) are shown.

Despite the inference of ballast water as responsible for the artificial dispersal of N. foveolatus in Paranaguá Estuarine Complex, the confirmation of this via of dispersal must be verified by additional studies. These could serve as alert on the species worldwide. The event can be the tip of the iceberg, representing a wide range of invasive species in the region (e.g.,Rocha & Kremer, 2005; Neves & Rocha, 2008; Lopes, 2009; Altvater & Coutinho, 2015).

Based only on the collection experience, it is already possible to infer that the specimens of N. foveolatus occur side by side with the native specimens of N. vibex, having the same niche. As previously only N. vibex existed in that place (Rios, 2009; Absher et al., 2015), at least a displacement of the native species has occurred. However, more ecological studies may certainly confirm this displacement and additional consequences in the local ecosystem, as nassariids can be predators and scavengers. Control procedures should be also greatly implemented.

ACKNOWLEDGEMENTS

We thank Esther Valentina da Veiga de Vasconcellos Gernet who collected the first specimens of N. foveolatus on the coast of Paraná state, two anonymous reviewers for their valuable comments in the manuscript, and Desyrêe Mathiew Teixeira Delgado for her help to edit Fig. 2.

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• Published with the financial support of the "Programa de Apoio às Publicações Científicas Periódicas da USP"

Appendix 1

Neighbor-Joining tree of the COI gene with all Nassarius sequences analyzed for genetic identification of the focal individual. Numbers in the nodes represent bootstrap values.

Appendix 2

Bayesian tree of the COI gene with all Nassarius sequences analyzed for genetic identification of the focal individual. Numbers in the nodes represent posterior probabilities.

Edited by

Edited by: Marcelo Veronesi Fukuda

Data availability

Data citations

Rosenberg, G. 2009. Malacolog 4.1.1: A Database of Western Atlantic Marine Mollusca. Available at: Available at: http://www.malacolog.org Access in: 24/04/2019.

Publication Dates

• Publication in this collection
  28 Nov 2019
• Date of issue
  2019

History

• Received
  19 July 2019
• Accepted
  07 Oct 2019