Introduction

The importance of the taxonomist work in biological and ecological research as well as in biodiversity management is well known, even though most of the time it is underestimated. Misidentification of specimens may have some consequences on the accuracy of ecological works and furthermore in fields like medicine, pharmacology, agriculture, conservation biology, ecosystem management and climatology (Dubois et al. 2013).

Some species may be also widely confused by “non-specialized” taxonomists with other similar but common species and this is a possible reason for their rareness.

Three cumaceans belonging to family Leuconidae Sars, 1878 are presented here as first record in the Adriatic Sea. Leuconidae is one of the earliest established cumacean families with no free telson, endopod of the uropod with two articles (rarely one) and which can occasionally have a functional eye (Watling 1991). Currently, the presence of Eudorella Norman, 1867 and Leucon Krøyer, 1846 genera in the Atlantic Ocean and in the Mediterranean basin (western Mediterranean, Ionian, Aegean and Levantine Seas) is documented by different authors (Lagardère, 1977; Elizalde et al. 1993; Gerken and Watling 1999; Madurell and Cartes 2003; Cartes et al. 2007, 2011; Fanelli et al. 2009; Mühlenhardt-Siegel 2009; Marusso 2010; Frutos and Sorbe 2014, 2017; Corbera and Sorbe 2020). Within the Mediterranean Sea these genera are represented by 3 (Eudorella) and 10 (Leucon) species (Marusso 2010), while only few studies reported them in the Italian waters (Graeffe 1902; Casellato et al. 2007; Casellato and Stefanon 2008; Klepal and Kastner 1980; Ligas et al. 2009; Coll et al. 2010).

Family Stenothoidae Boeck, 1871 was initially described, together with Amphilochidae Boeck, 1871, as a subfamily of Leucothoidae Dana, 1852 (Boeck 1871; Bousfield 1982), due to the presence in these families of very close characters at pereopods, uropods and mouthparts levels. Subsequently, Sars (1892) classified both Stenothoidae and Amphilochidae at family level (Krapp-Schickel and Koenemann 2006).

Among the 46 genera included within Stenothoidae the most represented is Stenothoe Dana, 1852 with 60 valid species already described, closely followed by Metopa Boeck, 1871 with 54 species (WoRMS Editorial Board 2020).

In 2006, Krapp-Schickel proposed a classification of the genus Stenothoe based on the presence of carinate body, prehensile pereopods and a naked or spinose telson. In 2015 the same author re-described the entire genus dividing the 55 valid species attributed since then in two groups: the largest one comprehending those species more similar to S. valida and the smaller one including those species similar to S. monoculoides (Krapp-Schickel 2015, 2006).

The genus Stenothoe is widely distributed all over the world from boreal to temperate regions (Myers 1985; Bellan-Santini 2005; Hayward and Morley 2005; Krapp-Schickel 2006; Krapp-Schickel et al. 2015; Krapp-Schickel and Lo Brutto 2015), both as free-living and in association with sea anemones (Vader 1984; Vader and Krapp-Schickel 1996; Krapp-Schickel 2015).

Up to date, only 14 out of 60 amphipods belonging to the genus Stenothoe are known to be distributed within the Mediterranean Sea (Marin and Sinelnikov 2018) and within them only S. bosphorana Sowinsky, 1898 is still considered as an endemic species (Krapp-Schickel 2015). There was only one old record of this species along the coast of Zlarin Island, Croatia (Krapp-Schickel 1976) without any further information since then.

The contribution of this paper is to rise the knowledge on the macrozoobenthos biodiversity, adding four smalls, but not less important, crustacean species to the Adriatic Sea fauna.

It is well known the importance of the biodiversity, to the point that the first descriptor of the “Good Environmental Status (GES)” of the EU Marine Strategy Framework Directive (MSFD; Directive 2008/56/EC) is, quoting: “Biological diversity is maintained. The quality and occurrence of habitats and the distribution and abundance of species are in line with prevailing physiographic, geographic and climate conditions”. In this contest, it is clear the role of taxonomists and the relevance of knowing the distribution of every single species in the biodiversity point of view; furthermore, to understand the spreading of some species (alien and/or invasive) due to climate changes and human activities is extremely crucial to have a clear picture of the native or already present species in a certain place.

Materials and Methods

Study Area

The Adriatic Sea is an elongated basin in the northernmost part of the Mediterranean, between the Italian Peninsula and the Balkans countries, with the major axis in the NW-SE direction. The northern area is very shallow, gently sloping, with an average depth of about 35 m, while the central part is on average 140 m depth, with 2 pits, the Pomo pit reaching ≈ 260 m and the South Adriatic pit reaching ≈ 1200 m. The northern and central parts of the basin are affected by a great number of rivers along the Italian coast, with the Po River being the most relevant in terms of water inflow (Artegiani et al. 1997). River runoff and wind stress are the main drivers of the water circulation. West Adriatic Current (WAC) and East Adriatic Current (EAC), flowing along the coasts, are the main currents affecting the Adriatic circulation. There are three main cyclonic gyres, one in the northern part, one in the middle and one in the south (Artegiani et al. 1997).

In the southern Adriatic Sea, the cyclonic gyre is observed in all seasons and a relatively strong western coastal current and a weaker eastern current are observed during summer. A strong annual thermal variation affects the northern and central Adriatic Sea and it is more pronounced at the surface (e.g., 5–28 °C) than close to the bottom (e.g., 12–17 °C). The water column from the coast to the 11–12 km offshore is characterized by low temperature (5–6 °C) and salinity (<37‰) in winter, while the offshore waters are warmer (10–12 °C) and thicker (>38‰). A vertical thermohaline front, parallel to the coast and extended throughout the water mass, divides the coastal waters from the open sea. In summer, instead, a horizontal stratification characterizes the water column, separating the warmer surface waters with lower salinity, from the deeper, colder and more saline ones (Artegiani et al. 1997).

The area is affected by a heavy marine traffic from cargo ships, supplier vessels for offshore activities (e.g., gas platforms), ferryboats, trawl-fishing vessels, cruise and recreational crafts (Coll et al. 2007; Pranovi et al. 2016). It is also characterized by intense mussel aquaculture along the Italian coast and by fish farming along the Croatian one (Ponti et al. 2007; Fabi et al. 2009).

Samples Collection and Analysis

Macrozoobenthos samples were collected during different surveys, from 2012 to 2019, within a multi-annual monitoring program aimed to assess the environmental effects of offshore gas extraction platforms.

Sampling was performed at three different square areas (A, B, C) of the central Adriatic Sea, each having a surface area of ≈ 16 km2 (Fig. 1; Table 1).

Fig. 1
figure 1

Geographical overview of the Adriatic Sea with the details of the surveyed areas

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Table 1 Survey areas with geographical position, mean depth and bottom type
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Twenty-four sites where randomly chosen within each area and six samples were collected at each site using a Van-Veen grab (capacity 13.0 L; surface 0.1 m2). The grab samples were sieved in situ through a 0.5 mm mesh, preserved in 5% buffered formalin and later transferred to 70% ethanol. Macrozoobenthos was sorted and identified in the laboratory using a stereomicroscope Zeiss Stemi 2000C and a compound microscope Zeiss Axiolab 5 equipped with eyepiece reticles, stage micrometers and camera.

The specimens herein examined and descripted are the first of the total recorded (Table 2) during the whole surveys period. All the specimens were measured in size (Total Body Length, TL), dissected when necessary, examined under higher magnification and identified following the below-mentioned systematic keys and descriptions.

Table 2 Specimens of E. nana, L. affinis, L. siphonatus and S. bosphorana recorded from 2012 to 2018 surveys in the three areas
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Bellan-Santini et al. (1993) and Krapp-Schickel (2015) for the amphipod and Bǎcescu (1951), Fage (1951), Jones (1976) and Shalla (2011) for the cumaceans were followed for the systematic keys and description.

For some individuals of each species, pictures of body parts were taken using Zeiss Axiocam ERC5s 5mpx. The handmade draws were obtained from the pictures, using XP-PEN Graphic Tablet Deco 02 Pen 8192 and Autodesk SketchBook software.

The nomenclature herein follows the World Register of Marine Species (WoRMS Editorial Board 2020). Voucher specimens are presently kept in the reference collection of CNR-IRBIM in Ancona, Italy.

Results

During the overall sampling period, 7 E. nana and 11 L. affinis were found in A and B areas, 274 L. siphonatus in A, B and C areas and 3 S. bosphorana were only found in C area (Table 2).

Systematic

Class Malacostraca Latreille, 1802.

Order Amphipoda Latreille, 1826.

Family Stenothoidae Boeck, 1871 .

Subfamily Stenothoinae Boeck, 1871 .

Genus Stenothoe Dana, 1852.

Stenothoe bosphorana Sowinsky, 1898.

Material examined: Three male specimens (cod. StB-1, StB-2, StB-3) collected in C area in 2018.

Diagnosis: The species presents a sexual dimorphism (Ruffo, 1993).

According to Bellan-Santini et al. (1993) and Krapp-Schickel (2015).

TL: 3.5–4.1 mm. Submarginal spines and marginal setae on the telson. Body smooth. Pereopods not prehensile. Eyes present. Antenna 1 and 2 long and slender. Gnatopod 1 feeble, propodus slender and oval, carpus free posterior margin parallel to the anterior one, palm undefined, merus a little shorter than carpus. Gnatopod 2 propodus strong, palm distally serrated with 5–6 protuberances (Fig. 2a). Pereopod 7 (P7) merus reaching distal end of carpus (Fig. 2b).

Fig. 2
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Stenothoe bosphorana Sowinsky, 1898. Male StB-1; a: Gn2, b: P7

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Ecology and distribution: S. bosphorana is known to live on muddy bottoms between 35 and 360 m (Bellan-Santini et al. 1993).

As above mentioned, S. bosphorana is still considered an endemic species in the Mediterranean Sea (Krapp-Schickel 2015), where it is distributed in the eastern part of the basin, from the Sea of Marmara and North Aegean Sea to the Levantine Sea (Krapp-Schickel 1976; Manoudis et al. 2005; Bakir et al. 2014). Fewer records were also registered in the western part of the Mediterranean, particularly in Saint-Tropez Gulf and alongside the Tunisian coast (Chevreux and Fage 1925; Zakhama-Sraieb et al. 2009).

Up to date, no further records are available in literature for this species, except for an uncertain one at the Azores which is still under debate (Krapp-Schickel 1976; Bellan-Santini 2005).

Order Cumacea Krøyer, 1846.

Family Leuconidae Sars, 1878.

Genus Eudorella Norman, 1867.

Eudorella nana Sars, 1879.

Material examined: Six female individuals (cod. EuN-1, EuN-2, EuN-3, EuN-4, EuN-5, EuN-6) collected in A area in 2012.

Diagnosis: According to Bǎcescu (1951), Fage (1951), Jones (1976) and Shalla (2011).

TL: 1.2–3.8 mm. Carapace anteriorly truncate without prominent pseudorostrum (Fig. 3); efferent orifice dorsal. Anterior lateral part of carapace shaped in an evident, horizontal, elongated tip forming a unique tooth in the male and few much shorter teeth in the female; immediately above, a V-shaped excavation with a single upwards pointed tooth on top; an evident sheaf of long bristles on the posterior margin of the fifth abdominal segment.

Fig. 3
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Eudorella nana Sars, 1879, female EuN-1, carapace

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Ecology and distribution: E. nana is considered typical of circalittoral habitats, living in different types of sediment, from sandy bottoms to coastal terrigenous mud, as well as in coastal detritic, muddy detritic, and shelf-edge detritic bottoms (Carpine 1970; Ledoyer 1983; Corbera and Cardell 1995). It is considered an endemic species recorded in the Western Mediterranean Sea (Fage 1940, 1951; Carpine 1970; Reyss 1972; Ledoyer 1983, 1987; Coll et al., 2010; Marusso 2010), in the Ionian Sea and in the Aegean Sea (Mühlenhardt-Siegel 2009; Reyss 1974).

Even though Watling (1991) questioned the validity of the species E. nana, he included it in the species list belonging to the genus, while Cartes and Sorbe (1997) did not separate the species E. nana and E. truncatula (Bate, 1856), considering both as E. truncatula. Several taxonomists still discriminate E. nana and E. trincatula as two different species (Fage, 1951; Carpine 1970; Reyss 1972; Ledoyer 1983; Corbera and Cardell 1995; Mühlenhardt-Siegel 2009; Coll et al., 2010; Marusso 2010; Koulouri et al. 2016; WoRMS Editorial Board 2020).

Genus Leucon Krøyer, 1846.

Subgenus Leucon Kroyer, 1846.

Leucon (Leucon) affinis Fage, 1951 .

Material examined: Six females (cod. LeAff-1, LeAff-2, LeAff-3, LeAff-4, LeAff-5, LeAff-6) collected in A area in 2012.

Diagnosis: According to Bǎcescu (1951), Fage (1951), Jones (1976) and Shalla (2011).

TL: 1.8–3.6 mm. Carapace 1/4 of the total length; pseudorostrum straight largely cut off at the top; dorsal ridge with an anterior batch of 16 contiguous teeth, followed by a smooth and concave depression and by another series of 4 teeth extending up to the rear edge of the carapace; peduncle of uropods with the same length of endopod, which is a little shorter than exopod.

Ecology and distribution: L. affinis is a bathyal species, living from 180 to 415 m depth (Mühlenhardt-Siegel 2009) in sandy bottoms and in deep-sea muds (Carpine 1970; Ledoyer 1983,1987; Corbera and Cardell 1995).

Some authors recorded this species in northeast Atlantic Ocean (Corbera and Sorbe 2020), in Western Mediterranean (Fage 1951; Carpine 1970; Reyss 1972; Ledoyer 1983; Mühlenhardt-Siegel 2009; Coll et al., 2010) and in Ionian and Levantine seas (Mühlenhardt-Siegel 2009; Coll et al., 2010), specifying that it might be confused with L. fulvus Sars, 1865 and L. acutirostris Sars, 1865, which are common in the northern Atlantic Ocean (Fage 1951; Gerken and Watling 1999).

Subgenus Macrauloleucon Watling, 1991 .

Leucon (Macrauloleucon) siphonatus Calman, 1905.

Material examined:

Sixteen female specimens (cod. LeSip-1, LeSip-2, LeSip-3, LeSip-4, LeSip-5, LeSip-6, LeSip-7, LeSip-8, LeSip-9, LeSip-10, LeSip-11, LeSip-12, LeSip-13, LeSip-14, LeSip-15, LeSip-16) collected in A area in 2012.

Diagnosis: According to Bǎcescu (1951), Fage (1951), Jones (1976) and Shalla (2011).

TL: 1.7–3.1 mm. Elongated branchial siphon developing from the front of pseudorostrum, accompanied by long bristles; dorsal and antero-lateral edge of carapace with some teeth; distal end of endopod with a long apical plumose bristle and four internal spines, exopod with internal and external bristles on margins.

Distribution: L. siphonatus is reported as a bathyal species, typical of sandy bottoms and deep-sea muds (Carpine 1970; Ledoyer 1987, 1983; Corbera and Cardell 1995).

It was recorded in the Atlantic Ocean, in the west coast of Iceland, Ireland, in the Bay of Biscay (Hansen 1920; Fage 1929; Reyss 1972; Gerken and Watling 1999; Corbera and Sorbe 2020), and in different areas of the Mediterranean Sea: Western Mediterranean Sea (Calman 1906; Fage 1940; Reyss 1972; Ledoyer 1987, 1983), Tyrrhenian, Ionian and Levantine Seas (Klepal and Kastner 1980; Madurell and Cartes 2003; Mühlenhardt-Siegel 2009; Coll et al., 2010).

Remarks

The A area bottom, with an average depth of 75 m, was characterized by sand (Shepard’s classification). The macrozoobenthos community herein was dominated by the following taxa: Ditrupa arietina (O. F. Müller, 1776), Sabellidae nd. Latreille, 1825, Prionospio cirrifera Wirén, 1883, Paraonidae nd. Cerruti, 1909 and Aphelochaeta filiformis (Keferstein, 1862). Area B, 75 m mean depth, was characterized by a silty-sand bottom and the dominant macrozoobenthos taxa were Paraonidae nd., Ophelina cylindricaudata (Hansen, 1879), Paradiopatra calliopae Arvantidis & Koukouras, 1997, Aphelochaeta filiformis and Prionospio cirrifera. The sea bottom of C area was mainly silty-sand with an average depth of 80 m. The most abundant taxa in the macrozoobenthos community herein were Paraonidae nd., Ophelina cylindricaudata, Prionospio cirrifera, Paradiopatra calliopae, Callianassa subterranea (Montagu, 1808) and Aphelochaeta filiformis.

Considering the amphipods and cumaceans associated with the species recorded in this paper, in the three areas A, B and C a total of 57, 71 and 60 taxa were respectively found (Table 3). E. truncatula was the most abundant species in both areas A and B. Ampelisca diadema (Costa, 1853) was one of the dominant species in all the considered areas, together with Phtisica marina Slabber, 1769 (A area), Harpinia dellavallei Chevreux, 1910 (B area), Paraphoxus oculatus (G. O. Sars, 1879) and Orchomene grimaldii Chevreux, 1890 (C area).

Table 3 Total amphipod and cumacean taxa recorded from 2012 to 2018 surveys in the three areas
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Discussion

The taxonomic misidentification issue plays an important role in the marine biodiversity management, especially for very small-sized marine species. Furthermore, genetic analysis on these specimens is problematic as the small and fragile body makes difficult to collect suitable samples.

This study is aimed to contribute to the knowledge on the families Leuconidae and Stenothoidae distribution. In fact, several authors, as well as both European Register of Marine Species (Costello et al. 2020) and World Register of Marine Species (WoRMS Editorial Board 2020), report the distribution of the four species here recorded in different areas of the Mediterranean Sea (Watling 2001; Coll et al. 2010; Watling and Gerken 2014; WoRMS Editorial Board, 2020) without any (or only one old record in the case of S. bosphorana) information on their presence in the Adriatic Sea; moreover the “Italian Checklist of Marine Fauna” (Marusso 2010) does not report E. nana and L. siphonatus in the Adriatic section, and L. affinis and S. bosphorana in all Italian seas.

Only 3 specimens of S. bosphorana were found in silty-sand bottom at 80 m depth in Adriatic Sea during the overall sampling period (from 2012 to 2019), highlighting the rareness of this species in this basin. Since this taxon was previously only reported living on muddy bottoms, this record adds a different bottom type where it can be found, also widening the living area.

The E. nana living habit fit with the environmental characteristics of the A and B areas where it was found, considered typical of the circalittoral zone and living in a wide range of bottom type, this record adds the Adriatic Sea to the E. nana living area, giving new information on its distribution.

In this study, L. affinis and L. siphonatus, until now considered as bathyal species living mainly on sandy and muddy deep-sea bottom, were found in shallow waters living in sand and silty-sand bottom of the Adriatic Sea, between 75 and 80 m depth, thus providing further information on their habitat and distribution.

The new record of the four species in the Adriatic Sea could be explained by the hypothesis that these species were already present in Adriatic, although not common, but had not yet been identified due to the poor knowledge about these taxa and the limited number of studies on these orders of crustacea, their small size and fragility and the difficulties to collect undamaged specimens using the common sampling techniques.

Further specific studies would be essential to better know the distribution of these taxa in this basin and therefore understand their ecological role in the benthic community.