Revision of deep-water species in Granulina (Gastropoda: Granulinidae) from Mauritania and Western Sahara

. Empty shells (thanatocoenoses) have been reviewed of species in the genus Granulina (Gastropoda: Granulinidae) from the lower shelf and upper bathyal zones off Mauritania and Western Sahara. We encountered nine species of which four were already known from off Mauritania. Four new species are proposed herein: Granulina reginae sp. nov., G. ronaldi sp. nov., G. sandrae sp. nov. and G. sigridae sp. nov. These four sympatric new species lack labial denticles and they probably form a phyletic clade with a common ancestor. Most hitherto known species in Granulina from the NE Atlantic Ocean and the Mediterranean possess labial denticles. One additional new species with denticles was left in open nomenclature because the material available was considered inadequate. Species in Granulina from Mauritania and Western Sahara have not been found off NW Morocco or the Canary Islands, and the species known from NW Morocco and the Canary Islands have not been found off Mauritania and Western Sahara. The southern extents of the distributions of the Mauritanian species are currently uncertain as additional sampling would be required off Senegal or further South. A key to Mauritanian species in Granulina is given.


Introduction
Staff at the Senckenberg am Meer Institute (Wilhelmshaven, Germany) studied the marine mollusk fauna from the upper slope and shelf of Mauritania and Western Sahara.In this paper, the gastropod genus Granulina Jousseaume, 1888 (family Granulinidae G. A. Coovert & H.K. Coovert, 1995) was studied in more detail.Species in the genus Granulina are relatively common in temperate waters around the world.Approximately 130 species are currently known in this taxon (MolluscaBase 2023).To date, there are fi ve species known from Mauritania.

R e s e a r c h a r t i c l e
urn:lsid:zoobank.org:pub:B09375C0-6E28-4E2D-BB7C-26E1753171E2 The granulinids from NW Africa have been described by various authors.Orbigny (1840) introduced Granulina guancha from Tenerife (Canary Islands).Locard (1897) described many new species from off NW Africa, including Granulina minusculina from off NW Morocco.Gofas (1992) reviewed the genus Granulina from NW Africa and the Mediterranean, and he described several new species, including G. africana from off Goree Island (Senegal) and G. mauretanica from Baie de l'Etoile, north of Nouadhibou, Mauritania.He also provided colour drawings of living animals of seven species, including G. mauretanica .Pin & Boyer (1995) described Granulina pierrepineaui from shallow water in Senegal.Boyer & Rolán (1999) introduced Granulina fernandesi from Boa Vista (Cape Verde Islands); this species showed a remarkable granular sculpture and it lacks labial denticles.Smriglio et al . (2000) described Granulina crassa , G. cerea , G. nofronii and G. crystallina from the shelf off northern Mauritania and Western Sahara.Boyer (2001) described Granulina canariensis from off Fuertaventura, Canary Islands.Finally, Boyer (2017) introduced the genus Granulinopsis Boyer, 2017 for small highly cylindrical granulinids that were originally placed in Granulina .Three species were included in Granuliopsis : G. cylindrata (Rolán & Boyer, 2004) from Senegal and Cape Verde, G. zanclea (Bogi, Boyer, Renda & Giacobbe, 2016) from the southern Tyrrhenian Sea and G. atlantidea (Boyer, 2016) from El Hierro, Canary Islands.Only G. cylindrata shows labial teeth within Granuliopsis , G. zanclea and G. atlantidea lack labial teeth.
Fossil species in Granulina are not well known from NW Africa.La Perna et al . (2001) reported on nine Pliocene granulinids from an outcrop near Estepona (western Mediterranean Sea, southern Spain); six species were extinct and three still occur today in the Mediterranean.
We were also able to fi nd new species among our samples and herein expand the knowledge of the genus Granulina off Mauritania and Western Sahara.The shells of the new species have no labial denticles but do possess a thickened lip.Labial denticles and a thickened lip are characteristic features in most known adult species of Granulina in the NE Atlantic and the Mediterranean Sea.Because of their different morphology, we consider them as adults of several new species.The absence of labial denticles was included as an identifi cation character.

Material and methods
This study focuses on the upper continental slope from Mauritania and Western Sahara.The material was collected using box cores or van Veen grabs during different expeditions.The German R/V Meteor cruises M36 (1975), M44 (1977), M53 (1980), and M60 (1982) sampled the lower shelf to the upper bathyal zone from NW Morocco to southern Mauritania.The Dutch CANCAP III (1978;van der Land 1987) and Tyro Mauritania I (1988)  The sediment samples were sieved on board and all size fractions greater than 0.5 mm were retained.They were subsequently washed with fresh water and dried.Live-collected samples were not available for this study.Therefore, we looked at shells from thanatocoenoses; live-collected yet dried specimens were only encountered occasionally in other genera.Examination of soft parts or genetic analyses could not be done.Judging from dating established on hard coral samples from the sea bottom, we assume that all shells are Recent (Late Holocene) to 90 kaBP (Late Pleistocene) age (Wienberg et al . 2018).All translucent shells are considered as Recent.
The material was sorted under a stereo microscope and the determinations were made using literature (particularly Gofas 1992;Smriglio et al . 2000).Selected (often translucent) shells were VON ELM L.-M. & HOFFMAN L., Granulina (Gastropoda) from NW Africa imaged using a Vega3-Tescan Scanning Electron Microscope (SEM).The shells were gold-coated to enhance the imaging of the micro-sculpture.Imaging was made using both secondary and backscatter electrons; incident electron energy was 20 keV.Shell measurements were made by using calibrated software in the SEM.All holotype specimens are stored in the Senckenberg Museum Frankfurt (SMF: Frankfurt am Main, Germany).Paratypes are stored in either SMF (Frankfurt am Main) or Naturalis Biodiversity Center (RMNH, formerly Rijksmuseum voor Natuulijke Historie, Leiden, the Netherlands).All other material is kept in SMF, RMNH or in Senckenberg am Meer (SaM, Wilhelmshaven, Germany).
The descriptions of new species are based on the photos of the type material illustrated herein.All illustrations of full shells have been made using the same magnifi cation.Sampled locations are stated by their coordinates in decimal format and depth in metres.

Granulina cerea
The holotype was deposited in the Bologna Zoology Museum (MZB14033).Smriglio et al . (2000) reported four shells from off Mauritania without further location details.Three paratypes were retained in private collections.Smriglio et al . (2000) indicated a shell height of 2.3 mm; the shells in our material show a height range for adult shells of 2.3-2.8mm.The species is a member of the four coffi n-shaped species from Mauritania.It has weak labial denticles, an angular outline and it lacks an (ab-)apical rostration.

Remarks
All species reported by Smriglio et al . (2000) as well as all other NE Atlantic and Mediterranean species investigated in this study show a micro-sculpture (ab-)apically, near the columellar folds, the parietal area and the outer lip.Smriglio et al . (2000) stated that his specimens did not show any micro-sculpture, even at high magnifi cation using a SEM.We note that the outline of a micro-sculpture is visible in some of their SEM images and colour photographs.
The species is known from empty shells in the latitudinal range between 17.0° N and 25.2° N. The full bathymetric range is 14-483 m; it is commonly found on the lower shelf at depths of 80-210 m in silty sand.Gofas (1992: fi g. 14) shows a small (height 2.15 mm) specimen from a depth of 50 m off Gorée Island (Senegal) under the name Granulina sp. which could belong to G. cerea .If confi rmed, then this would extend the southern distribution range signifi cantly.Smriglio, Gubbioli & Mariottini, 2000 Figs      2000) indicated a holotype height of 1.9 mm; our set indicates a maximum height of 2.1 mm.The species is the smallest member of the four coffi n-shaped species from Mauritania.It has very weak labial denticles that occasionally may be absent, even though these specimens may be subadult.Granulina crassa lacks an (ab-)apical rostration.

Granulina crassa
The species is known from empty shells in the latitudinal range 17.0-25.2°N. The full bathymetric range is 13-505 m; it is commonly found on the lower shelf at depths of 80-210 m in silty sand.

Remarks
The present species is similar to Granulina crassa but its outline is less elongated and less angular and its callus is very well developed across the apex, base and the parietal area.The three shells show a great variability in outline; possibly we deal with more than one species.
We refrain from proposing a new species as we identifi ed only three shells, two of which are eroded.The bathymetric range is 87-208 m; the latitudinal range is 17.0-17.3°N, off Nouakchott.The species is known from empty shells in the latitudinal range 17.0-20.3°N. It was found at depths of 30-1252 m in silty sand or mud.We could not confi rm the species occurring off Western Sahara.

Etymology
The name (feminine) of the species acknowledges the late Regina Albert, formerly a technical assistant at Senckenberg, who washed and sieved the raw Meteor samples and partly performed the preliminary sorting.

Description
Apex with widely convex, sharp, wide channel; outer lip smooth, thickened from apex to base, protruding and somewhat bevelled at periphery, reclining towards apex and base, internally smooth (without Four oblique folds at base of straight columella, folds unconnected and with rounded margins when young, upper two folds coalescent, forming vertical rim when adult.Parietal area widely convex and smooth.Macroscopic sculpture smooth with microscopic irregular growth lines; microscopic sculpture of fl akes oriented towards exterior on callus of external lip, columella and columellar folds, base and apex, callus reclining in the middle part; internally smooth.Aperture curved, elongated, narrowest above periphery, wide at base and at apex.Protoconch not visible, convolved inside shell.

Remarks
All described species of Granulina from north of Senegal have labial denticles and none have a wide apical channel in the aperture.Therefore, the present species cannot be confused with Granulina nofronii , G. crassa , G .crystallina or G .cerea (Smriglio et al . 2000), even though they have a relatively VON ELM L.-M. & HOFFMAN L., Granulina (Gastropoda) from NW Africa similar form.The new species Granulina reginae sp.nov.lacks labial denticles as do the other three new species: Granulina ronaldi sp.nov., G. sigridae sp.nov.and G. sandrae sp.nov.Compared to these species, G. reginae is smaller and somewhat broad (width/height ratio 0.64), clearly more rostrated and has a wide channelized apex, which the other new species do not have.Granulina sandrae is pearshaped and infl ated (width/height ratio 0.69), and G .ronaldi and G .sigridae are more elongated (width/ height ratio 0.56-0.59).Shells from juveniles are identifi ed by their sharp convolving lip and four separated columellar folds; adults have a thickened, bevelled lip and the upper columellar folds are coalescent.Coalescent folds probably are a gerontic character.
Many samples containing these new species were taken in coral rubble and mud.Most likely, they live in upper bathyal coral-associated habitats.Bathymetric range is 440-505 m; their latitudinal range is 17.6-20.3°N.

Etymology
The name (masculine) of the species acknowledges Ronald Janssen, retired curator of the Mollusca collection in the Senckenberg Museum Frankfurt who salvaged the Meteor material when it was about to be discarded and who initiated the preservation and sorting process.He also allowed us to study the Meteor samples.

Description
Apex with highly convex, blunt, narrowing channel.External lip smoothly rounded, strongly thickened from apex to base, maximum convexity slightly above periphery, reclining towards apex and base, widely channelled at highly convex base, pointed at base columella, internally smooth (without labial denticles).Four discrete oblique folds at base of straight columella, with round edges, third fold longest.Parietal area widely convex and smooth.Macroscopic sculpture smooth with microscopic irregular growth lines; microscopic sculpture of fl akes oriented towards exterior on callus of external lip, columella, columellar folds, base and apex, callus reclining in the middle part; internally smooth.Aperture curved, elongated, wide at base.Protoconch invisible, convolved inside shell.

Remarks
Because of the missing labial denticles, this species cannot be mistaken for any hitherto known species found north of Senegal.The morphology is similar to Granulina occulta but that species has labial denticles.The outline of the present species is not as broad (width/height ratio 0.59) as in Granulina sandrae sp.nov.(width/height ratio 0.69) and it has a narrow aperture.Granulina reginae sp.nov.has a wide, notched apical channel and its last whorl is widely rounded at the periphery.
Granulina ronaldi sp.nov.could be mistaken for G. sigridae sp.nov.but that species has different columellar folds; the two upper ones are often coalescent and the third one is not as long as the fourth one.The micro-sculpture in the present species covers a wider area at the base of the callus and apex and is not as retracted in the parietal area as in G. sigridae either .The outer lip of the present species is more thickened, with weaker convexity and slightly angular.The (ab-) apical outlines are more convex than in G. sigridae .La Perna et al . (2001) described the similar Granulina longa La Perna, Landau & Marquet, 2001 from the Pliocene near Estepona (western Mediterranean, Spain).Granulina longa differs from the present species by a well-rounded oval outline, a wide aperture and a thin lip with fi ne labial denticles.La Perna et al . (2003) described another similar species: Granulina choffati La Perna, Landau & da Silva, 2003 from the Atlantic Pliocene in Portugal.It is differentiated from the present species by fi ne labial denticulations, and a more oval outline.
The bathymetric range is 81-411 m.The latitudinal range is 18.9-25.4°N, which is the northernmost occurrence of the new species.Some shells were found in sandy or muddy silt occasionally with other shells.The habitat of the species is uncertain.Granulina sandrae sp.nov.urn:lsid:zoobank.org:act:1D97D3ED-F5D5-466B-9008-C0B9F63CAEAFFigs 5, 8

Etymology
The name (feminine) of the species acknowledges Sandra Müller, technical assistant at the Senckenberg Museum Frankfurt, who has been the key person incorporating the SaM samples into the SMF collection.

Description
Apex with highly convex, blunt, narrowing channel.External lip smoothly rounded, thickened from apex to base, protruding and maximum convexity well above periphery, reclining towards apex and base, internally smooth, without labial denticles.Four spiral folds at base of straight columella, upper two folds coalescent but still distinct.Parietal area widely convex and smooth.Macroscopic sculpture smooth with microscopic irregular growth lines; microscopic sculpture of fl akes oriented towards exterior on callus of external lip, columella and columellar folds, base and apex, callus reclining in the middle part; internally smooth.Aperture curved, elongated, narrowest at periphery, wide at base and narrower at apex.Protoconch invisible, convolved inside shell.

Remarks
Granulina boucheti Gofas, 1992 shows a morphological similarity to the new species; it has a similar size and outline but it differs by its labial denticles on the inside of the external lip; the present species lacks labial denticles.Granulina sigridae sp.nov.has a wide channel with less convex margin apically, and it is more elongated (width/height ratio 0.56 versus 0.69 in G. sandrae sp.nov. ) with an even convexity in the outer lip.
The Pliocene Granulina iberica La Perna, Landau & Marquet, 2001 has a similar outline as the present species but it differs by the presence of fi ne labial teeth, a widely notched apical channel and an obliquely truncated apical outline.The present species shows a tapered apex.

Etymology
The name (feminine) of the species acknowledges Sigrid Hof, technical assistant at the Senckenberg Museum Frankfurt, who performed the preliminary sorting of the Meteor samples.

Description
Apex with weakly convex, blunt, narrowing channel.External lip smoothly rounded, thickened from apex to base, protruding and maximum convexity slightly above periphery, reclining towards apex and base, widely channelled at highly convex base, pointed at base columella, internally smooth (without labial denticles).Four spiral folds at base of straight columella, upper two folds are coalescent yet distinct.Parietal area widely convex and smooth.Macroscopic sculpture smooth with microscopic VON ELM L.-M. & HOFFMAN L., Granulina (Gastropoda) from NW Africa irregular growth lines; microscopic sculpture of fl akes oriented towards exterior on callus of external lip, columella and columellar folds, base and apex, callus reclining in parietal area; internally smooth.Aperture curved, elongated, narrowest and maximum curvature at apex, wide at base.Protoconch invisible, convolved inside shell.

Remarks
Similar to the other new species, Granulina sigridae sp.nov.has no labial denticles, but the shell morphology is different.The shell is not as wide (width/height ratio 0.56) as in G. sandrae sp.nov.(0.69) and it lacks the widely fl ared apical channel like in G. reginae sp.nov.Granulina sigridae is similar to G. occulta but that species has labial denticles and it lacks the wide channel at the base.Granulina ronaldi sp.nov.has separated columellar folds, an apex with more convexity, a base that is more tapered, and has a thicker lip.
The bathymetric range is 200-548 m; the latitudinal range is 17.4-20.4°N. Most of the specimens were found in coral rubble with mud and an association with upper bathyal coral-related habitats is likely.

Key to Mauritanian species in Granulina
This key is for small (< 5 mm) ovoid convolved shell with an internal protoconch.

Discussion
Nine species of Granulina were present in our samples, of which four are new: G. reginae sp.nov., G. ronaldi sp.nov., G. sigridae sp.nov.and G. sandrae sp.nov.One species was left in open nomenclature ( G. aff .crassa ) because the available material was inadequate.Four species were already described by Smriglio et al . (2000): G. cerea, G. crassa, G. crystallina and G. nofronii.VON ELM L.-M. & HOFFMAN L., Granulina (Gastropoda) from NW Africa West African fauna.Ekman (1953) placed the interface between the European and western African biotic regions further South at Cap Vert.Briggs (1974) placed the interface further north at Cap Blanc, his bioregions were based on fi sh distribution data.Costello et al . (2017) studied global bioregional zones on a very large faunal data set.Their analyses provided insuffi cient resolution to distinguish the NW African biotic regions.Our distribution data show Mauritanian species in Granulina extending north to Western Sahara but not extending into NW Morocco.Additionally, species in Granulina known from NW Morocco or the Canary Islands have not been found off Mauritania or Western Sahara.The distributions of species of Granulina adhere to the biotic regions shown in Caballero Herrera et al . (2022).The southern limits of the distribution ranges are currently poorly defi ned as we did not have access to deep-water samples south of Mauritania.
expeditions sampled the shelf off northern Mauritania.The German R/V Poseidon 346 cruise (2007; Westphal 2007) concentrated on the coral mounds off central and southern Mauritania (Banda and Timiris mound complexes).The German R/V Maria S. Merian cruise MSM 16/3 (2010; Westphal et al .2014) sampled the shelf of the Banc d'Arguin and the deep-water coral mound chains off Mauritania.

Fig. 5 .
Fig. 5. Location map of the new species in Granulina Jousseaume, 1888 off Mauritania and Western Sahara.White circles show all investigated stations; colour symbols show locations of shells from new species.Granulina reginae sp.nov. is presented by yellow squares, G. sigridae sp.nov.as red diamonds, G. sandrae sp.nov.as blue triangles, and G. ronaldi sp.nov.as green circles.Bathymetric data from GEBCO; contours 500 m

Banc d'Arguin •
5 shells; 20.3667° N, 17.6667° W; depth 200 m; 28 Oct. 1978; CANCAP stn 3.120; sandy clay with shells; van Veen grab; RMNH.MOL.351803• 12 shells; The species is a largest member of the four coffi n-shaped species from Mauritania.It has weak labial denticles, a clear angular outline and it shows a weak (ab-)apical rostration.The species is known from empty shells in the latitudinal range 17.0-21.4°N.It is commonly found on the lower shelf at depths of 52-210 m in silty sand.RemarksSmriglio et al .(2000) indicated a holotype height of 2.4 mm; our set indicates a maximum height of 2.5 mm.The species has an elliptical or weak coffi n-shaped outline; it has strong labial denticles, and it lacks rostration.A similar species is Granulina choffati La Perna, Landau & da Silva, 2003 from the Atlantic Pliocene in Portugal.It is differentiated from G. nofronii by a fi ner labial denticulation.