The point on Opaliopsis atlantis (Gastropoda: Epitoniidae) distribution: new data from the Mediterranean and implications

Abstract

Specimens of the rare amphi-Atlantic epitoniid Opaliopsis atlantis have been recorded in the Strait of Messina (central Mediterranean) from a hydrozoan stylasterid-rich habitat. The record, which adds a new site to the sporadic occurrences of this prevalently deep-water species, may be considered the first contextualized report from Mediterranean Sea. Opaliopsis atlantis displays a planktotrophic larval development functional for long-range colonization of favorable habitats. Its discontinuous distribution all over its broad geographic range highlights the potential role of Atlantic seamounts as stepping-stones for transoceanic dispersal. Although no conclusive information is yet available upon the feeding requirements of O. atlantis all over its range, we suggest that this cnidarian-ectoparasitic prosobranch could adapt to different hosts, as a strategy that may enhance its wide biogeographic distribution.

Key-Words.
Epitoniidae; Amphi-Atlantic; Mediterranean; Bathyal; Biogeography

INTRODUCTION

Opaliopsis atlantis (Clench & Turner, 1952) belongs to a kind of epitoniids provided with a multispiral and ribbed planktotrophic larval shell. This morphologically distinct deep-water group, previously placed in the subfamily Nystiellinae Clench & Turner, 1952, was then elevated to family level by Nützel (1998), until subsequent biomolecular studies did not validate their separation from Epitoniidae (Takano & Kano, 2014; Bouchet & Rocroy, 2017). The planktotrophic development, involving a high dispersal ability (Bouchet & Warén, 1986), accounts for the number of “nystiellids” displaying an amphi-Atlantic distribution (Lima & Christoffersen, 2013). Originally described upon few specimens from Cuba and Florida, O. atlantis was reported also off Brazil (Andrade et al., 2011; Lima & Christoffersen, 2013). To the east, O. atlantis is known from Azores, Madeira and Gibraltar (Bouchet & Warén, 1986; de Frias Martins et al., 2009; Segers et al., 2009; Gofas et al., 2014) up to the Mediterranean (Smriglio & Mariottini, 1999; Mifsud, 2009; Manousis et al., 2018). O. atlantis is one of the most uncommon epitoniids, known thus far from a handful of live specimens and a few empty shells all over its range. The finding of two specimens from the Strait of Messina (central Mediterranean) improves our knowledge on the areal of this rare species and suggests some considerations on its ecology.

MATERIAL AND METHODS

Samplings were carried out in July-August 1995 by means of modified Van Veen grab (0.25 m² sampling surface) and triangular dredge (60 cm mouth opening), according to the expected sea-floor nature. Samples were washed on board, under a gentle seawater flow throughout 1 mm mesh sieve, and residues fixed in alcohol 70%. The living fauna was sorted in laboratory under a stereomicroscope, while the residual sediment was dried at room temperature. A first specimen of O. atlantis (Messina University; repository code: BEL145POP’95FRAN1) was found in a crab sample from a steep canyon head belonging to the Gioia Basin system (Longhitano, 2018), north-east sector of Messina Strait (St. FRAN1; 38°22′26.83″N, 15°37′40.40″E; 389 m depth). Soft tissue remains recognizable throughout the shell aperture were extracted and examined under stereomicroscope. A second specimen (Coll. Renda, Amantea; repository code: CWR145POP’95RAN10) was found in the residue from the sample RAN10 (38°14′58″N, 15°37′37″E), from 110 to 80 m depth, dredging a vertical cliff in the “Sill”, a site located transversely to the Strait in its narrowest point and characterized by rough topography with pinnacles (Longhitano, 2018) (Fig. 1).

Figure 1
Bathymetric map of the northern Messina Strait (modified from Doglioni et al., 2012). The two O. atlantis sampling stations are indicated.

Abbreviations: BEL = Benthic Ecology Laboratory, University of Messina, Italy; CFS = Collection Franck Swinnen; CWR = Collection Walter Renda, Amantea, Cosenza, Italy; CWS = Collection Willy Segers; MCZ = Museum of Comparative Zoology, Cambridge, USA; MMF = Museu Municipal do Funchal, Madeira, Azores; MNRJ = Museu Nacional/Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil; MZSP = Museu de Zoologia/Universidade de São Paulo, São Paulo, Brazil; USNM = National Museum of Natural History, Washington, DC, USA; ZMA = Zoologisch Museum Amsterdam.

RESULTS

The specimen from station RAN10 (Figs. 2A-C, 3A-B) was found associated to almost 2 dm³ biogenic coarse residue, consisting of fragments of the stylasterid Errina aspera (Linnaeus, 1767) infested by the ectoparasite gastropod Pedicularia sicula Swainson, 1840. The specimen, lacking the protoconch, measured 9.0 mm in teleoconch length.

Figure 2
(A-F) Opaliopsis atlantis: (A-C) Shell from Station CWR145POP’95RAN10, height 9.0 mm. (D-F) Shell from Station BEL145POP’95FRAN1, heigh 8.4 mm.

Figure 3
(A-D) Opaliopsis atlantis, details of apex and aperture. (A-B) CWR145POP’95RAN10; (C-D) BEL145POP’95FRAN1.

The specimen from station FRAN1 (Figs. 2D-F, 3C-D) was found associated to a biostromal framebuilding formed by deep-sea oysters, Neopycnodonte cochlear (Poli, 1795). The specimen, also lacking in protoconch, measured 8.4 mm in length. The organic matter found inside the shell, lacking operculum as well as other recognizable tissues, might belong to sipunculid remains.

DISCUSSION

The scant information available on O. atlantis mostly refers only on a generic geographic location. For instance, general information about depth and geographical coordinates has been provided for holotype and paratypes, with the indication “off Lantana in 83 fathoms” of McGinty collection paratype. Nothing is reported about habitat and specimen condition, although the original description, reporting operculum features, suggests that the type at least was collected alive (Clench & Turner, 1952). Other West Atlantic reports, only providing depth and geographical coordinates, concerned empty shells from Brazil (Andrade et al., 2011). To the east, the statement “The species may be still living in the E. Atlantic” by Bouchet & Warén (1986) about their record from Azores implies that the specimen was not collected alive (some inaccuracy on the BALGIM 153 position was later clarified in Bouchet & Taviani, 1989). Further records of dead specimens and fragments by Brenke (2002), Segers (2009), de Frias Martins et al. (2009), were occasionally supported by depth and/or geographic position (Table 1).

Table 1
Synoptic table of O. atlantis reports from scientific literature. Geographical coordinates and depths are reported according to the original data.

Code	spm	Locality	Position	Depth m	Reference	Additional data
		West Atlantic
MCZ 187988	1 alive	Bahia de Cochinos, Cuba	22°09'N - 81°10'W	420-484	Clench & Turner, 1952	Holotype
	1	Lantana, Florida		152	Clench & Turner, 1952	Paratype - McGintypriv. coll.
USNM 417386	1	Key West, Florida		115	Clench & Turner, 1952	Paratype - Eolis station 43
USNM	1	Key West, Florida, USA		118	Clench & Turner, 1952	Paratype - Eolis station 321
MNRJ 13617	1	Ceará, Brasil	02°14'25"S - 38°22'50"W	240-260	Andrade et al., 2011
MZSP 67621	1	Ceará, Brasil	02°14'25"S - 38°22'50"W	240-260	Andrade et al., 2011
MNRJ 15499	1	Pernambuco, Brasil		690	Andrade et al., 2011
MNRJ 13615	1 shell	Santa Catarina, Brasil	26°38'44.9"S - 06°51'54.2"W	150	Andrade et al., 2011
MNRJ 13613	1	Santa Catarina, Brasil	26°38'44.9"S - 46°51'54.2"W	150	Andrade et al., 2011
		East Atlantic
	1 shell	Azores	37°35'N - 25°32'W	810-825	Bouchet & Waren, 1986	BIACORESexpedition ST 240
		Gran Meteor Banck	30°00'N - 28°30'W		Brenke, 2002	Meteorexpedition M42/3
MMF 33280	1 shell	Madeira		54	Segers et al., 2009	SEPLAT expedition st 133
CFS	1 shell	Madeira			Segers et al., 2009	SEPLAT expedition st 133
CWS	fragment	Porto-Novo, Madeira,		364	Segers et al., 2009
ZMA	fragment	Deserta Grande		120	Segers et al., 2009	CANCAP expedition st 1017
	1 shell	Azores	37°41'34" N - 25°27'34"W	167-189	de Frias Martins et al., 2009
		Mediterranean
	4 (würmian?)	Strait of Gibraltar	35°53'N - 06°33'W	518-524	Bouchet & Waren, 1986	BALGIM expeditionDR49
	1 (würmian?)	Strait of Gibraltar	35°53'N - 06°32'W	518-526	Bouchet & Waren, 1986	BALGIM expeditionDW50
	1 (würmian?)	West Alboran Sea	35°56'N - 05°35'W	568-604	Bouchet & Waren, 1986	BALGIM expedition DR153
	2 shells	Alboran Sea, Spain	36°21.06'N - 03°58.07'E	349-365	Gofas et al., 2014	DEEPER 04/09 cruise
	1 shell	Central Tyrrhenian Sea	41°24'N - 12°03'E	500-600	Smriglio & Mariottini, 1999	Private collection
	2 shell	Malta	35°56'N - 14°19'E	140-160	Mifsud, 1993
	1 dead	Malta	35°57.934'N - 14°10.706'E	550	Mifsud, 2009
	1 alive, 5 shells	North Aegean		200-400	Manousis et al., 2018
BEL145POP'95FRAN1	1 dead	Strait of Messina, Italy	38°22'26.83"N - 15°37'40.40"E	389	Present paper	POP'95 expedition St. FRAN1
CWR145POP'95RAN10	1 dead	Strait of Messina, Italy	38°14'58"N - 15°37'37"E	80-110	Present paper	POP'95 expedition St. RAN10

In the Mediterranean, more information is given by Bouchet & Warén (1986) which hypothesize that their contextualized records from Gibraltar and Alboran pertain to last glacial (Würmian) submarine deposits. Sporadic dead specimens have been reported as associated with continental slope bioconstructions at 500-600 m depth (Smriglio & Mariottini, 1999) and Leptometra community (Gofas et al., 2014; see figure in Rueda et al., 2019), respectively from the Tyrrhenian Sea and the Alboran Sea. Depth and generic indications of “rocky and coralliferous” habitats are given by Manousis et al. (2018), about occasional records of one living specimen and five shells from North Aegean. More important, the occasional record of a living specimen from Malta’s continental slope with “fossil” deep water corals (Mifsud, 2009) documents that O. atlantis in the Mediterranean is ectoparasitic on the actinarian Actinauge richardi (Marion, 1882).

Such host-parasite relationship, however, seems limited to the situation observed in the Strait of Messina, where the habitat of A. richardi (Pierdomenico et al., 2019) overlaps that of O. atlantis, whilst this actinarian is unknown in the west Atlantic fauna. A potential implication is that O. atlantis is not strictly species-specific, suggesting that, similarly to other ectoparasites, it is not tied to a peculiar habitat, but could exploit other cnidarians in its geographic range. Nothing however is known about the West Atlantic habitat of O. atlantis, except for the bathymetric range that agrees with the Mediterranean records (Table 1).

Opaliopsis atlantis is also known as fossil in lower circalittoral to bathyal Pleistocene deposits facing the Strait of Messina (Crovato & Taviani, 1985), as well as in nearby north-eastern Sicily (Di Geronimo et al., 2005). As far as concerns the amphi-Atlantic distribution of O. atlantis, first comments are given by Crovato & Taviani (1985), which favor the hypothesis of a Mediterranean settlement by vertical migrating larvae rather than through a step-by-step bottom colonization. Such a hypothesis is consistent with the recognized ability of some tropical gastropod species to ensure an amphi-Atlantic distribution by means of long-living teleplanic larvae. The planktotrophic development, moreover, has been indicated as a functional adaptation in prosobranch gastropods inhabiting transient habitats such as sunken wood and hydrothermal vents, more in general seeming most suited for exploitation of patchy but widespread habitats (Jablonski & Lutz, 1983).

At least two Amphiatlantic-Mediterranean coralliophilinae ectoparasitic on deep water corals, Coralliophila richardi (Fischer, 1882) and Babelomurex sentix (Bayer, 1971), similarly, illustrate the role of the seamounts as stepping-stones in transoceanic dispersal (Oliverio & Gofas, 2006). The physiographic setting of the seamounts, in this respect, plays a fundamental role, due to little sedimentary input and extensive hard bottoms in the bathyal, similarly to the Messina Strait environment (Longhitano, 2018). Regarding C. richardi,Taviani et al. (2009) suggest its status of permanent resident in the western Mediterranean, in accordance with “its prolonged, albeit not necessarily continuous, presence in this basin since the Early Pleistocene”. A situation somehow analogous for O. atlantis, whose presence in the Strait of Messina area is documented since the Pleistocene (Crovato & Taviani, 1985).

The scattered records of O. atlantis, covering a wide bathymetric range, concern different benthic assemblages that include the here reported oyster beds and bathyal stylasterids Errina aspera, a peculiar habitat that the Strait of Messina shares with Gibraltar and, throughout the vicariant E. dabneyi (Pourtalès, 1871), with the East Atlantic Azores islands (Braga-Henriques et al., 2011).

CONCLUSION

The present records in the Strait of Messina confirm further the amphi-Atlantic distribution and basinal-wide occurrence of O. atlantis in the Mediterranean Sea. The report, which after Bouchet & Warén (1986) and Gofas et al. (2014) for Gibraltar and Alboran, is the first to arise from a planned investigation, rather than from occasional records, suggests that this species is not an occasional visitor from the Atlantic Ocean as it has been hypothesized for most deep-sea gastropods (see Bouchet & Taviani, 1989). Opaliopsis atlantis, instead, should be considered a component of the Mediterranean fauna since long (Pleistocene), as testified by its fossil record in this basin.

The planktotrophic larval development in principle permits the distribution of this species over a wide geographic range accounting for its presence in the western Atlantic. The few eastern Atlantic records refer to seamounts underlining their role as stepping-stones for prosobranch amphi-Atlantic dispersal (Leal & Bouchet, 1991; Brenke, 2002), up to include the Mediterranean Sea (Gofas et al., 2014). Ectoparasitic prosobranchs, like O. atlantis, could be able to exploit such corridors adapting to different habitats and communities. This situation might imply a certain plasticity with respect to feeding requirements which could contemplate different hosts.

ACKNOWLEDGEMENTS

Investigations were carried out in the framework of the “POP’95 Regional Program”, aimed to define zonation and distribution of benthic communities in the Strait of Messina. Our thanks go to Marco Taviani (CNR, Bologna, Italy) for the precious suggestions.

REFERENCES

• Andrade, B.G.; Costa, P.M.S. & Pimenta, A.D. 2011. Taxonomic review of the genus Opaliopsis (Gastropoda: Nystiellidae) from Brazil, with description of a new species. Journal of the Marine Biological Association of the United Kingdom, 91(7): 1561-1566.
• Bouchet, P. & Rocroy, J.P. 2017. Revised classification, nomenclator and typification of gastropod and monoplacophoran families. Malacologia, 61(1-2): 1-526.
• Bouchet, P. & Taviani, M. 1989. Atlantic deep sea Gastropods in the Mediterranean: new findings. Bollettino Malacologico, 25(5-8): 137-148.
• Bouchet, P. & Warén, A. 1986. Revision of the North Eastern Atlantic bathyal and abyssal Aclididae, Eulimidae, Epitoniidae (Mollusca:Gastropoda). Bollettino Malacologico, Supplemento, 2: 297-576.
• Braga-Henriques, A.; Carreiro-Silva, M.; Porteiro, F.; Matos, V.; Sampaio, Í.; Ocaña, O. & Ávila, S.P. 2011. The association between a deep-sea gastropod Pedicularia sicula (Caenogastropoda: Pediculariidae) and its coral host Errina dabneyi (Hydrozoa: Stylasteridae) in the Azores. ICES Journal of Marine Science, 68(2): 399-407. http://doi.org/10.1093/icesjms/fsq066
  » http://doi.org/10.1093/icesjms/fsq066
• Brenke, N. 2002. The benthic community of the Great Meteor Bank. In: Oceanography and Ecology of Seamounts - Indications of Unique Ecosystems. ICES ASC CM 2002/M:30, 1-12.
• Clench, W.J. & Turner, R.D. 1952. The genera Epitonium (Part II), Depressiscala, Cylindriscala, Nystiella and Solutiscala in the western Atlantic. Johnsonia, 2(31): 289-356.
• Crovato, P. & Taviani, M. 1985. Nystiella atlantis Clench & Turner, 1952, from the Pleistocene of Archi (Reggio Calabria: Southern Italy): first fossil record of the subfamily Nystiellinae (Gastropoda, Epitoniidae). Bollettino Malacologico, 21(10-12): 289-294.
• de Frias Martins, A.M.; Borges, J.P.; Ávila, S.P.; Costa, A.C.; Madeira, P. & Morton, B. 2009. Illustrated checklist of the infralittoral molluscs off Vila Franca do Campo. Açoreana, Suplemento, 6: 15-103.
• Di Geronimo, I.; Messina, C.; Rosso, A.; Sanfilippo, R.; Sciuto, F. & Vertino, A. 2005. Enhanced biodiversity in the deep: Early Pleistocene coral communities from southern Italy. In: Freiwald, A. & Roberts, J.M. (Eds.). Cold-water corals and ecosystems. Berlin, Springer-Verlag. p. 61-86.
• Doglioni, C.; Ligi, M.; Scrocca, D.; Bigi, S.; Bortoluzzi, G.; Carminati, E.; Cuffaro, M.; D’Oriano, F.; Forleo, V.; Muccini, F. & Riguzzi, F. 2012. The tectonic puzzle of the Messina area (Southern Italy): Insights from new seismic reflection data. Scientific Reports, 2: 970. http://doi.org/10.1038/srep00970
  » http://doi.org/10.1038/srep00970
• Gofas, S.; Salas, C.; Rueda, J.L.; Canoura, J.; Farias, C. & Gil, J. 2014. Mollusca from a species-rich deep-water Leptometra community in the Alboran Sea. Scientia Marina, 78(4): 537-553. http://doi.org/10.3989/scimar.04097.27A
  » http://doi.org/10.3989/scimar.04097.27A
• Jablonski, D. & Lutz, R.A. 1983. Larval ecology of marine benthic invertebrates: paleobiological implications. Biological Reviews of the Cambridge Philosophical Society, 58: 21-89.
• Leal, J.H. & Bouchet, P. 1991. Distribution patterns and dispersal of prosobranch gastropods along a seamount chain in the Atlantic Ocean. Journal of the Marine Biological Association of the United Kingdom , 71: 11-25.
• Lima, S.F.B. & Christoffersen, M.L. 2013. Nystiellidae (Gastropoda: Epitonioidea) collected during the REVIZEE Program/Northeast Brazil with descriptions of new species and a checklist of the Family from the Atlantic Coast of South America. American Malacological Bulletin, 31(2): 289-296.
• Longhitano, S.G. 2018. Between Scylla and Charybdis (part 1): the sedimentary dynamics of the modern Messina Strait (central Mediterranean) as analogue to interpret the past. Earth-Science Reviews, 18: 59-287. http://doi.org/10.1016/j.earscirev.2018.06.008
  » http://doi.org/10.1016/j.earscirev.2018.06.008
• Manousis, T.; Kontadakis, C.; Polyzoulis, G.; Mbazios, G. & Galinou-Mitsoudi, S. 2018. New marine gastropod records for the Hellenic waters. Journal of Biological Research-Thessaloniki, 25: 6. http://doi.org/10.1186/s40709-018-0077-3
  » http://doi.org/10.1186/s40709-018-0077-3
• Mifsud, C. 1993. Recent Mediterranean findings, Opaliopsis atlantis (Clench& Turner, 1952). La Conchiglia, 25(268): 61-62.
• Mifsud, C. 2009. Opaliopsis atlantis (Clench & Turner, 1952) (Gastropoda: Epitoniidae) found on an actiniarian in the Mediterranean Sea. Bollettino Malacologico, 45(1): 1-3.
• Nützel, A. 1998. Uber die Stammesgeschichte der Ptenoglossa (Gastropoda). Berliner Geowissenschaftliche Abhandlungen, ser. Berliner Geowissenschaftliche Abhandlungen, ser E (Palaeobiologie), 26: 1-229.
• Oliverio, M. & Gofas, S. 2006. Coralliophiline diversity at mid-Atlantic seamounts (Neogastropoda, Muricidae, Coralliophilinae). Bulletin of Marine Science, 79(1): 205-230.
• Pierdomenico, M.; Cardone, F.; Carluccio, A.; Casalborne, D.; Chiocci, F.; Maiorano, P. & D’Onghia, G. 2019. Megafauna distribution along active submarine canyons of the central Mediterranean: Relationships with environmental variables. Progress in Oceanography, 171: 49-69.
• Rueda, J.L.; Urra, J.; Aguilar, R.; Angeletti, L.; Bo, M.; García-Ruiz, C.; González-Duarte, M.M.; López, E.; Madurell, T.; Maldonado, M.; Mateo-Ramírez, Á.; Megina, C.; Moreira, J.; Moya, F.; Ramalho, L.V.; Rosso, A.; Sitjà, C. & Taviani, M. 2019. Cold-Water Coral Associated Fauna in the Mediterranean Sea and Adjacent Areas. In: Orejas, C. & Jiménez, C. (Eds.). Mediterranean cold-water corals: past, present and future. Coral Reefs of the World. Cham, Springer. v. 9, p. 295-333. http://doi.org/10.1007/978-3-319-91608-8_29
  » http://doi.org/10.1007/978-3-319-91608-8_29
• Segers, W.; Swinnen, F. & De Prins, R. 2009. Marine molluscs from the Portuguese province of Madeira. Madeira and Selvagens Archipelago. Monoplacophora, Polyplacophora, Gastropoda, Bivalvia & Scaphopoda. Belgium, Snoeck Publishers. 612p.
• Smriglio, C. & Mariottini, P. 1999. Molluschi del mar Tirreno centrale. Contributo XII. Segnalazione di due rari Epitoniidae batiali per le coste Laziali. Bollettino Malacologico, 34(9-12): 137-140.
• Takano T. & Kano Y. 2014. Molecular phylogenetic investigations of the relationships of the echinoderm-parasite family Eulimidae within Hypsogastropoda (Mollusca). Molecular Phylogenetics and Evolution, 79: 258-269.
• Taviani, M.; Angeletti, L.; Dimech, M.; Misfud, C.; Freiwald, A.; Harasewych, M.G. & Oliverio, M. 2009. Coralliophilinae (Gastropoda: Muricidae) associated with deep-water coral banks in the Mediterranean. The Nautilus, 123(3): 106-112.

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Edited by: Marcelo Veronesi Fukuda

Publication Dates

• Publication in this collection
  04 Dec 2020
• Date of issue
  2020

History

• Received
  11 Aug 2020
• Accepted
  14 Oct 2020
• Published
  16 Nov 2020