Checklist of free-living nematode species in the transitional environment of Lake Varano (Southern Italy)

Abstract

Checklist of free–living nematode species in the transitional environment of Lake Varano (Southern Italy)
This study documents for the first time the taxonomic composition of the nematode community and the number of free–living nematode species in Lake Varano, Southern Adriatic Sea, Italy. The nematode community was mainly composed of species typical of fine sediments that usually prevail in transitional environments (TE). An overall high number of nematode species was recorded (55), belonging to 36 genera in 17 families. These values are highly comparable to those reported for other Italian TE, but appear lower than those recorded in other European brackish–water systems, probably in relation to the low salinity range of Lake Varano. Forty taxa were identified up to species level, thus increasing the number of the nematode marine species known for the Italian coasts from 443 to 463, for the Adriatic basin from 310 to 313, and for the Southern Adriatic sector from 37 to 77. Considering the importance of this phylum in the assessment of ecological quality and the great vulnerability of the Adriatic Sea ecosystems, an intensification of sampling efforts should be planned, especially in the Central–Southern part of the basin. Such a plan would provide new insights into the biogeography of one of the most important components of the benthic domain and potentially yield new information about the climate warming effects on the Adriatic Sea.

Data published through GBIF [doi:10.15470/xktjni]

Key words: Free–living nematodes, Biodiversity, Transitional environments, Southern Adriatic Sea

Resumen

Lista patrón de especies de nematodos de vida libre en el ambiente de transición del lago Varano (sur de Italia)
Este estudio documenta por primera vez la composición taxonómica de la comunidad de nematodos y el número de especies de nematodos de vida libre presentes en el lago Varano, al sur del mar Adriático (Italia). La comunidad de nematodos estaba compuesta principalmente por especies típicas de los sedimentos finos predominantes en ambientes de transición (TE). En conjunto, se registró un elevado número de especies de nematodos (55) pertenecientes a 36 géneros de 17 familias. Estos valores son comparables en gran medida a los registrados en otros TE italianos, pero inferiores a los registrados en otros sistemas de aguas salobres europeos, probablemente en relación con el bajo nivel de salinidad del lago Varano. Se identificaron cuarenta taxones a nivel de especie, lo que incrementa el número de especies conocidas de nematodos marinos en las costas italianas de 443 a 463, en la cuenca del Adriático de 310 a 313 y en el sur del mar Adriático de 37 a 77. Considerando la importancia de este fílum para la valoración de la calidad ecológica y la gran vulnerabilidad de los ecosistemas del mar Adriático, debería planificarse la intensificación de las acciones de muestreo, especialmente en la parte centro-meridional de la cuenca. Un plan de este tipo proporcionaría nuevos conocimientos de la biogeografía de uno de los componentes más importantes del bentos y podría aportar nueva información acerca de los efectos del calentamiento climático en el mar Adriático.

Datos publicados en GBIF [doi:10.15470/xktjni]

Palabras clave: Nematodos de vida libre, Biodiversidad, Ambientes de transición, Sur del
mar Adriático

Resum

Llista patró d’espècies de nematodes de vida lliure a l’ambient de transició del llac Varano (sud d’Itàlia)
Aquest estudi documenta per primera vegada la composició taxonòmica de la comunitat de nematodes i el nombre d’espècies de nematodes de vida lliure presents al llac Varano, al sud de la mar Adriàtica (Itàlia). La comunitat de nematodes estava composta principalment per espècies típiques dels sediments fins predominants en ambients de transició (TE). En conjunt, es va registrar un nombre elevat d’espècies de nematodes (56) pertanyents a 36 gèneres de 17 famílies. Aquests valors són comparables en gran mesura amb els registrats en altres TE italians, però inferiors als registrats en altres sistemes d’aigües salabroses europeus, probablement en relació amb el baix nivell de salinitat del llac Varano. Es van identificar quaranta taxons a nivell d’espècie, la qual cosa incrementa el nombre d’espècies conegudes de nematodes marins a les costes italianes de 443 a 463, a la conca de l’Adriàtica de 310 a 313 i al sud de la mar Adriàtica de 37 a 77. Atesa la importància d’aquest fílum per a la valoració de la qualitat ecològica i la gran vulnerabilitat dels ecosistemes de la mar Adriàtica, s’hauria de planificar la intensificació de les accions de mostreig, especialment a la part centre-meridional de la conca. Un pla així proporcionaria nous coneixements de la biogeografia d’un dels components més importants del bentos i podria aportar nova informació sobre els efectes de l’escalfament climàtic a la mar Adriàtica.

Dades publicades a GBIF [doi:10.15470/xktjni]

Paraules clau: Nematodes de vida lliure, Biodiversitat, Ambients de transició, Sud de la
mar Adriàtica

Introduction

Transitional environments (TEs) are aquatic systems characterized by large fluctuations of physicochemical and geochemical variables that could  greatly affect the benthos (Barnes et al., 2008; Frontalini & Coccioni, 2011). The Adriatic Sea coast, in particular, hosts a large amount of TEs, ranging from the largest and most studied Lagoon of Venice to wetlands, estuaries, embayments and ponds. All these habitats have been modified to meet human requirements for millennia and are currently under severe stress due to anthropogenic activities and climate change (Airoldi & Beck, 2007).

The phylum Nematoda is the most diverse and numerically dominant component of the aquatic ecosystems (Balsamo et al., 2010; Appeltans et al., 2012). It is particularly important to study TEs due to its ability to survive during environmental changes that may reduce or eliminate macrobenthos (Hendelberg & Jensen, 1993). Furthermore, nematodes are well recognized as a useful tool for biomonitoring assessment of marine ecosystems (Balsamo et al., 2012; Semprucci et al., 2015). Many studies of meiofaunal communities have been carried out in Italian TEs, but they generally concern a higher taxonomic level of identification (Colangelo & Ceccherelli, 1994; Colangelo et al., 1996; Guerrini et al., 1998; Fiordelmondo et al., 2003; Gambi et al., 2003; Fabbrocini et al., 2005; Pusceddu et al., 2007; Cibic et al., 2012).

The species of marine nematodes known in the Italian seas are 443 and are distributed into 262 genera and 46 families (Semprucci et al., 2008). Since the total number of Italian species is a quarter of that of species recorded along European coasts, the overall level of knowledge for the Italian Seas can be considered good. However, these data were collected in the early the 20^th century and should be updated (Semprucci, 2013). Furthermore,  studies on nematode communities are scarce in  southern Italy and have mainly been focused around genus level (De Zio, 1964, 1966; Grimaldi-De Zio, 1967, 1968a, 1968b; De Leonardis et al., 2008; Sandulli et al., 2010, 2011). This is also true for the only information available on the nematodes of the Lesina Lagoon, a southern Italian TE (Fabbrocini et al., 2005).

Lake Varano is a coastal lagoon located on the northern side of the Gargano National Park (Southern Adriatic Sea). It comprises an area of about 65 km² and its water depth is about 4 m (Spagnoli et al., 2002). The lake is fed  by two artificial channels (Capoiale and Varano) connecting it with the Adriatic Sea and by two tributaries (Antonino and San Francesco Canals) bringing fresh waters from the catchment area. However, the range of salinity range in Lake Varano is  generally  low  (from 23.0 to 31.9) (Frontalini et al., 2013).

In this paper, we list the species and their distribution both at a global and local scale.  We also discuss the state of knowledge of Nematoda from the Adriatic basin and southern Italy along with the TE.

Material and methods

Sediment samples from 21 stations were collected on 22nd March 2012 using a modified model of Van Veen Grab (fig. 1). Samples  were treated with a 7% MgCl₂ aqueous solution to narcotize the fauna, fixed in a 4% formaldehyde solution in buffered sea-water, and stained with Rose Bengal. In the laboratory, the samples were rinsed with a gentle jet of fresh water through a 0.5 mm sieve to remove the macrofaunal components. The residual sediment was then decanted, sieved 10 times through a 42 μm mesh and centrifuged three times with Ludox HS30 (specific density 1.18) (Pfannkuche & Thiel, 1988). One hundred nematodes were randomly picked from each sample and mounted on permanent slides for taxonomic study (Seinhorst, 1959). The specimens were observed under Nomarski Differential Interference Contrast illumination (Optiphot-2 Nikon, 100x oil immersion objective) and identified by means of the NeMys online identification key (Vanaverbeke et al., 2015). The list of nematode species reported below follows Hodda (2011) for the taxonomic status and the Nemys website for the relative geographical global distribution: in the cases for which updates of the latter were available specific references are cited in the Results section. The distribution of nematode species along the Italian coasts refers to Semprucci et al. (2008), while the recording localities in Adriatic Sea relate to Travizi & Vidaković (1997) and Semprucci (2013). All the nematode specimens studied are deposited in the collection of the Zoology Laboratory of the University of Urbino (Italy).

Fig. 1. Map of the study area with location of sampling stations. Fig. 1. Mapa del área de estudio y localización de los emplazamientos de muestreo.

Results

Fifty-five nematode species belonging to 36 genera and 17 families were found at Lake Varano (table 1). Data published through GBIF: doi:10.15470/xktjni. The richness ranged from 4 (V29) to 27 (V7) species per station.

Table 1. List per station of the free–living nematode species found in Lake Varano (Southern Adriatic Sea, Italy). Tabla 1. Lista de nematodos de vida libre registrados en las distintas estaciones de muestreo del lago Varano (sur del mar Adriático, Italia).

The richest families were Chromadoridae (10 species), Linhomoeidae (9) and Xyalidae (8), followed by Oncholaimidae (5), Comesomatidae (3), Cyatholaimidae (3), Microlaimidae (3), Axonolaimidae (2), Camacolaimidae (2), Desmodoridae (2), Leptolaimidae (2), Anoplostomatidae (1), Diplopeltidae (1), Monhysteridae (1), Oxystominidae (1), Selachinematidae (1) and Sphaerolaimidae (1).

Fifteen taxa were identified as putative species because the specimens collected were juveniles or females, which often lack the diagnostic features required for an accurate taxonomic identification. However, their records are shown in table 1 because they contribute to the few available data for the Southern Adriatic coasts.

The list of species identified is given below:

Order Enoplida Filipjev, 1929
Family Anoplostomatidae Gerlach & Riemann, 1974

Anoplostoma viviparum (Bastian, 1865) Bütschli, 1874

Geographical distribution: North Sea, Baltic Sea, Black Sea, Gulf of Mexico, Mediterranean Sea, North Atlantic Ocean, Azov Sea. In Italy this species was originally reported for the Northern Adriatic Sea where it was known only in the Po Delta and the Venice Lagoon.
Ecological notes: the species was found in the southern part of the lake in sediments with a prevalent fraction of mud (mud: 66-68%, sand: 32-34%) and a level of organic matter (CaCO₃ content) ranging from 34 to 44%.

Order Oncholaimida Siddiqi, 1983
Family Oncholaimidae Filipjev, 1916

Oncholaimus brevisetosus Kreis, 1932

Geographical distribution: Indian Ocean (Indonesia). The species is the first record for Italy.
Ecological notes: the species was collected in a western station of the lake. The sediments were characterized by a prevalent amount of mud (58%) and the CaCO₃ content was high (81%).

Oncholaimus longicaudatus (Kreis, 1932) Rachor, 1969

Geographical distribution: Indian Ocean. This is the first record for Italy.
Ecological notes: it was found in front of the Capoiale Channel. The sediments were sandy deposits (sand: 63%; mud: 41%) characterized by 41% of CaCO₃.

Oncholaimellus mediterraneus Stekhoven, 1942

Geographical distribution: Mediterranean Sea, North Atlantic Ocean, North Sea. Sergeeva (1977) also reported this species from the Black Sea. In Italy, it was reported for the South Tyrrhenian Sea and the Northern Adriatic Sea: here it was recorded at Mirna Estuary, Rovinj area and Makarska harbour area (Croatia).
Ecological notes: it was collected only in the station in front of the Capoiale Channel. The substratum consisted of sandy sediments (sand: 63%; mud: 41% ) with a 41% fraction of CaCO₃.

Order Chromadorida Chitwood, 1933
Family Chromadoridae Filipjev, 1917

Chromadora yamadai Kito, 1978

Geographical distribution: North Pacific Ocean. This is the first record for Italy.
Ecological notes: it was found especially in front of the Capoiale and Varano Channels and was associated with  sediments with a prevalent fraction of sand (sand: 53-73%; mud: 27-47) and  a generally rich amount of organic matter (CaCO₃: 28-63%).

Chromadorella macris (Gerlach, 1956) Lorenzen, 1972

Geographical distribution: South Atlantic Ocean. This is the first record for Italy.
Ecological notes: this species was scarce in the study area. It was mainly found in sandy sediments and only in one case in sediments with a dominance of mud (St. 31) (range of sand: 16-90%; mud: 10-84%). It was generally associated with relatively high levels of CaCO₃ (10-56%).

Chromadorella salicaniensis Boucher, 1976

Geographical distribution: North Sea and Adriatic Sea. It was found in  the Venice Lagoon (Northern Adriatic Sea).
Ecological notes: it was not abundant in the study area and found only at two stations close to the baymouth bar. It was collected mainly from sandy sediments (sand: 73-90%; mud: 10-27%) characterized by a low level of CaCO₃ (10-28%).

Chromadorina germanica (Bütschli, 1874) Wieser, 1954 

Geographical distribution: Mediterranean Sea, North Atlantic Ocean, North Sea. In particular, it was known in Italy only for the Ligurian and Northern Tyrrhenian coast.
Ecological notes: it was more frequent in the northern-central part of the lake. It was related to sediments characterized by a roughly equal fraction of sand and mud (39-68% and 32-61%, respectively). The amount of CaCO₃ was variable, ranging from 23 to 81%.

Neochromadora papillosa Pastor de Ward, 1985

Geographical distribution: West Atlantic. This is the first record for the Italian coasts.
Ecological notes: it was found in few stations, all in the eastern part of the lake, mainly in muddy sediments (sand: 32-65%; mud: 35-68%) with a generally high organic content (CaCO₃: 10-48%).

Neochromadora poecilosomoides (Filipjev, 1918) Micoletzky, 1924

Geographical distribution: Black Sea, Mediterranean Sea, North Atlantic Ocean, North Sea. The previous reports in the Italian coasts were from the Ligurian and Southern Tyrrhenian Seas, Strait of Messina, the south-eastern tip of Sicily and the northern part of the Adriatic sector (Rovinj area).
Ecological notes: it was found in several stations, but especially in the northern part of the lake and mainly in relation to the sand fraction (sand: 16-90%; mud: 10-84%).  The amount of CaCO₃ varied from 9.5 to 80%.

Ptycholaimellus macrodentatus (Timm, 1961) Wieser & Hopper 1967

Geographical distribution: Bay of Bengal. It is the first record in Italy.
Ecological notes: it was mainly collected from the marginal zones of the lake, in sediments ranging in sand percentage from 16 to 73% and in mud from 27 to 84%. The CaCO₃ level varied from 10 to 81%.

Spilophorella euxina Filipjev, 1918

Geographical distribution: Black Sea, Mediterranean Sea, North Atlantic Ocean. The Adriatic sector was the only part of the Italian coasts reported to host this species (offshore area of the Rovinj –Po River mouth and Poreć– Venice transects, Lim Channel, Rovinj area and Raśa Bay, Croatia).
Ecological notes: it was collected only in front of the Varano Channel in association with sandy sediments (sand: 73%; mud: 27%) with a relatively poor organic content (28% of CaCO₃).

Family Cyatholaimidae Filipjev, 1918

Cyatholaimus gracilis (Eberth, 1863) Bastian, 1865

Geographical distribution: Black Sea, Mediterranean Sea, North Atlantic Ocean, North Sea. The presence of this species is well documented on the Italian coasts: Ligurian and Southern Tyrrhenian Seas, Strait of Messina, Northern Adriatic Sea (Po Delta, Rovinj area, Gulf of Trieste) and Central Adriatic Sea (Fiorenzuola and Brisighella).
Ecological notes: it was found only in front of the baymouth bar, in sandy sediments (sand: 90%; mud: 10%) with a very low organic content (10% of CaCO₃).

Paracanthonchus longicaudatus Warwick, 1971

Geographical distribution: Barents Sea, North Atlantic Ocean, North Sea. It is the first record for Italy.
Ecological notes: it was found in only two stations,  associated with  sandy sediments (sand: 53-90%; mud: 10-47%). The level of CaCO₃ varied from 10 to 63%.

Order Selachinematida Hodda, 2011
Family Selachinematidae De Coninck, 1965

Synonchiella edax Aissa & Vitiello, 1977

Geographical distribution: Mediterranean Sea. It is a new record for the Italian coasts.
Ecological notes: it was located especially in the northern and central part of the lake. The sediments were mainly characterized by a dominant sandy component (from 39 to 90%) with a medium-low organic content (CaCO₃ from 10 to 63%).

Order Desmodorida De Coninck, 1965
Family Desmodoridae Filipjev, 1922

Desmodora granulata Vincx & Gourbault, 1989

Geographical distribution: France (Morlaix, Brittany). This is a new record for Italy.
Ecological notes: it was found only in front of Capoiale Channel in sandy sediments (sand: 63%; mud: 41%), with 41% of CaCO₃.

Molgolaimus allgeni (Gerlach, 1950) Jensen, 1978

Geographical distribution: North Atlantic Ocean, North Sea and Adriatic Sea (Rovinj –Po River mouths and Venice).
Ecological notes: it was detected in almost all the stations of the study area and was   one of the most abundant species. It was mainly associated with the fine sediment fraction (sand: 32-73%; mud: 27-84%) and organic enrichment (CaCO₃: 10-81%).

Family Microlaimidae De Coninck & Stekhoven, 1933

Aponema torosa (Lorenzen, 1973) Jensen, 1978

Geographical distribution: North Atlantic Ocean, North Sea. In the Adriatic Sea, it was reported for the Northern sector (Lim Channel and Raśa Bay, Croatia).
Ecological notes: it was one of the most widespread species in the lake, but it was especially abundant in front of the two channel) and in the central parts of the lake. Sediments were muddy (mud fraction from 37 to 84%; sand fraction from 16-65%) and usually contained a high level of organic matter (CaCO₃ from 10 to 81%).

Microlaimus honestus De Man, 1922 (op. Kovalyev & Tchesunov, 2005)

Geographical distribution: Argentina (Fuegian Archipelago), Baltic Sea, English Channel, Mediterranean Sea, North Atlantic Ocean, North Sea, South Atlantic Ocean, Southern Ocean (Antarctic Ocean, Graham Island, King George Island, South Weddell Sea), Uruguay, East Pacific.
In Italy it was reported only for the Tyrrhenian coasts. The present finding is a new record for the Adriatic Basin.
Ecological notes: this species was found in almost all stations, but especially in front of two channels and in the central part of the lake. Sediments were mainly muddy (mud: 27-84%; sand: 16-73%) and salinity levels ranged from 23 to 30‰.

Order Monhysterida Filipjev, 1929
Family Axonolaimidae De Coninck & Stekhoven, 1933

Axonolaimus caudostriatus Boucher, 1973

Geographical distribution: Pacific Ocean (Polynesian islands). It is a new record for the Italian coasts.
Ecological notes: the species was found only in the area close to the baymouth bar and mainly in sandy sediments (sand: 43-90%; mud: 10-57%) with a CaCO₃ level from 10 to 27%.

Odontophora wieseri Luc & De Coninck, 1959

Geographical distribution: North Atlantic Ocean. In Italy, it was previously known only in the Central Adriatic Sea.
Ecological notes: it was collected in few stations, mainly located in the northern part of the lake. It was strongly associated with the sandy fraction of the sediment (sand: 42-90%; mud: 10-58%) and a low organic content (CaCO₃: 10-81%).

Family Comesomatidae Filipjev, 1918

Paracomesoma dubium (Filipjev, 1918) Stekhoven, 1950

Geographical distribution: Mediterranean Sea, North Atlantic Ocean. In Italy, it was only known in the Northern Adriatic Sea (in the Venice Lagoon) and Bakar Bay, Croatia.
Ecological notes: it was collected from the northern part of the lake, and in particular in sandy sediments (sand: 43-73%; mud: 27-57%) with a medium level of organic matter content (CaCO₃ : 27-28%).

Sabatieria pulchra (Schneider, 1906) Riemann 1970

Geographical distribution: Baltic Sea, Black Sea, Mediterranean Sea, North Atlantic Ocean, North Sea. In the Northern Adriatic Sea it was reported for: Po Delta, Venice Lagoon (Italy) Mirna Estuary, Raśa Bay and Makarska harbour area (Croatia).
Ecological notes: species abundant and widespread in the area. It was mainly related to fine sediments (mud: 35-84%; sand: 16-65%) in conjunction with levels of salinity from 23 to 30‰.

Sabatieria pomarei (Boucher, 1973) Jensen, 1979

Geographical distribution: South Pacific Ocean (Polynesia). This is a new record for the Italian coasts.
Ecological notes: It was found only in the station in front of the Capoiale Channel, in sandy sediment (sand: 63%; mud: 41%) characterized by 41% of CaCO₃.

Family Linhomoeidae Filipjev, 1922

Metalinhomoeus biformis Juario, 1974

Geographical distribution: Adriatic Sea (Po River mouth and Venice Lagoon in Venice, Rovinj, Mirna Estuary, Lim Channel, Rovinj area and Makarska harbour in Croatia).
Ecological notes: it was found in only one station at the western part of the lake, with 57% of sand and 43% of mud, and 54% of CaCO₃.

Metalinhomoeus musaecauda Lorenzen, 1966

Geographical distribution: North Atlantic Ocean and North Sea. It is the first record in Italy.
Ecological notes: it was found in a few stations, mainly located in the Southern part of the lake and in front of the Capoiale Channel. It was collected from sediments characterized by a prevalent mud component (from 47 to 68%), while the sand fraction was generally lower (32-53%). The level of CaCO₃ ranged from 34 to 63%.

Terschellingia brevicauda Ott, 1972

Geographical distribution: North Atlantic Ocean (North Carolina). It is the first record in Italy.
Ecological notes: it was found mainly in the northern and western part of the lake in sediments characterized by a prevalent sandy component (sand: 32-73%; mud: 27-68%) and a medium-high level of organic content (27-63%).

Terschellingia communis De Man, 1888

Geographical distribution: Mediterranean Sea, North Atlantic Ocean and North Sea. In the Adriatic Sea, it was recorded at the offshore area of the Rovinj –Po River mouths and Poreć– Venice transects, Po Delta, Venice Lagoon, Mirna Estuary, Lim Channel, Rovinj area, Raśa Bay and Makarska harbour area.
Ecological notes: it was found only in the central and eastern part of the lake. It was mainly associated with sediments, with a sand percentage from 44 to 65% and mud from 35 to 56%. The level of organic matter content ranged from 21 to 48%.

Terschellingia longicaudata De Man, 1907

Geographical distribution: Baltic Sea, Barents Sea, Gulf of Mexico, Mediterranean Sea, North Atlantic Ocean, North Sea and New Zealand zone. Ürkmez et al. (2011) also reported its presence in the Black Sea. In the Adriatic Sea, it was reported in the offshore area of the Rovinj –Po River mouth and Poreć– Venice transects, Po Delta, Venice Lagoon, Mirna Estuary, Lim Channel, Rovinj area, Raśa Bay, Makarska harbour area and South Adriatic (eastern coasts).
Ecological notes: it was abundant and frequent in all the stations of the lake. It was found in sediments with ranges of sand from 16 to 63% and mud from 27 to 84%. The range of CaCO₃ was 10 to 81%.

Terschellingia vestigia Gerlach, 1963

Geographical distribution: Indian Ocean (Maldives). It is the first record from Italy.
Ecological notes: it was recorded in a single station in the central part of the lake, with sandy sediments (sand: 60%; mud: 40%) and a medium level of organic matter (25% of CaCO₃).

Family Monhysteridae De Man, 1876

Thalassomonhystera parva (Bastian, 1865) Jacobs, 1987

Geographical distribution: North Atlantic Ocean, North Sea. It is the first record in Italy.
Ecological notes: it was well distributed in the lake, but more abundant in the eastern part. It was associated with sediments mainly represented by mud (32-68%) and sand (32-68%). The organic content varied from 10 to 81% and the species was related to salinity levels ranging from 23 to 29‰.

Family Sphaerolaimidae Filipjev, 1918

Sphaerolaimus gracilis De Man, 1876

Geographical distribution: Black Sea, Mediterranean Sea, North Atlantic Ocean and North Sea. In the Northern Adriatic sector, it was reported in the offshore area of the Rovinj –Po River mouth and Poreć– Venice transects and Rovinj area.
Ecological notes: it was collected from the stations close to Capoiale and Varano Channels and in the south-eastern part (see San Antonio Canal). It was found in sediments with a generally high level of mud (range from 37 to 84%) and low level of sand (16 to 63%) and an organic content that ranged from 10 to 44% of CaCO₃.

Family Xyalidae Chitwood, 1951

Daptonema curticauda (Tchesunov, 1980) Tchesunov, 1990

Geographical distribution: Caspian Sea. It is a new record for the Italian coasts.
Ecological notes: it was found in a few stations, mainly located in the northern part of the lake (Varano Channel) and at one station on the western coast. The species was associated with a prevalent mud component (mud: 43-61%; sand: 39-57%) and a generally high amount of organic matter (CaCO₃: 31-56%).

Daptonema fistulatus (Wieser & Hopper, 1967) Lorenzen, 1977

Geographical distribution: Gulf of Mexico, North Atlantic Ocean and North Sea. Its presence is documented in the shallow sublittoral of the central Adriatic coast (Fiorenzuola and Brisighella).
Ecological notes: it was frequently found in the northern and south-western part of the lake. It appeared associated with muddy sediments (mud: 37-61%; sand: 42-63%) with organic detritus (CaCO₃: 27-81%).

Daptonema normandicum (De Man, 1890) Lorenzen, 1977

Geographical distribution: France (Wimereux), Mediterranean Sea, North Atlantic Ocean, North Sea. In Italy its presence was documented by Guerrini et al. (1998) in the ‘Valli di Comacchio’ complex (Northern Adriatic Sea).
Ecological notes: it was frequent and abundant in the Varano Lake and was particularly abundant in the stations close to the San Francesco output and in the central area. It was present in sediments characterised by 27-84% of mud and 16-73% of sand, and appeared more abundant in sites with a low salinity level.

Paramonhystera pellucida (Cobb, 1920) Wieser 1956

Geographical distribution: North Pacific Ocean (California), Arabian Sea. This is the first record in Italy.
Ecological notes: it was collected only near the baymouth bar in relation to sandy sediments (sand: 90%; mud: 10%) with a poor organic content (CaCO₃: 10%).

Steineria simplex Timm, 1963

Geographical distribution: Arabian Sea. This is the first record in Italy.
Ecological notes: it was collected only at one station located on the eastern edge of the lake, in sandy sediments (sand: 65%; mud: 35%) with a high organic content (48%).

Order Plectida Malakhov, Ryzhikov & Sonin, 1982
Family Camacolaimidae De Coninck & Stekhoven 1933

Diodontolaimus sabulosus Southern, 1914

Geographical distribution: North Atlantic Ocean. This is the first record for Italy.
Ecological notes: this species was found only in the area close to the baymouth bar and in particular in sandy sediments (sand: 63%; mud: 41%) with 41% of CaCO₃.

Order Leptolaimida Hodda, 2007
Family Leptolaimidae Oerley, 1880

Leptolaimus luridus Timm, 1963

Geographical distribution: North Atlantic Ocean. This is a first record for the Italian coasts.
Ecological notes: it was one of the most abundant and widespread species in the lake, closely associated to muddy sediments (mud: 27-84%; sand: 16-73%) rich in organic detritus (CaCO₃: 10-81%).

Leptolaimus elegans (Stekhoven & De Coninck, 1933) Gerlach, 1958

Geographical distribution: North Atlantic Ocean, North Sea. In Italy, it was reported for the Southern Tyrrhenian coasts.
Ecological notes: it was found in a few stations on the eastern side of the lake, in muddy sediments (mud: 68-84%; sand: 16-32%). CaCO₃ ranged from 18 to 44%.

Discussion

Given its particular physico-chemical features, the Adriatic Sea  is strongly influenced by meteorological conditions and river discharges, and it is particularly sensitive to human impact and climatic changes (Occhipinti-Ambrogi et al., 2005; Balsamo et al., 2010; Frontalini et al., 2011).

However, the biodiversity of the Adriatic macrofauna does not appear to have suffered a substantial decrease during the last years, mainly because alien species have masked the overall species loss, but the trophic web and the functioning of marine ecosystems have been affected (e.g., Occhipinti-Ambrogi, 2002, 2007; Giani et al., 2012).

If it is relatively easy to document the changes in macrofaunal communities over time, it is not possible to do the same for meiofaunal organisms since their spatial distribution is frequently understudied in many geographical regions (Balsamo et al., 2010). Even when data are available, they are often outdated, making it difficult to determine biogeographic patterns or to support possible hypotheses of ‘tropicalization’ of the Adriatic Sea (Artois et al., 2011; Semprucci, 2013). The significance of the present study is that it provides a detailed list of nematode species from a littoral area of the Southern Adriatic Sea and updates knowledge on the Mediterranean regions.

Of the 55 species identified in the present study, 20 are new records for the Italian coasts, three are new records for the Adriatic basin, and 40 are reported for the first time for the Southern Adriatic sector (Semprucci et al., 2008). These data greatly increase our faunistic knowledge about  the distribution of marine Nematoda along the Italian coasts, and especially in the TE systems that are still poorly known environments.

The nematode community of Lake Varano mainly comprised species representative of fine sediments (Heip et al., 1985; Travizi & Vidakovic, 1997) or TEs (Villano & Warwick, 1995; Pallo et al., 1998; Fabbrocini et al., 2005; Barnes et al., 2008). The richness values were overall highly comparable to those reported for other Italian TEs (Guerrini et al., 1998; Fabbrocini et al., 2005), but were generally lower than those found in the European brackish water systems (e.g. Hendelberg & Jensen, 1993; Barnes et al., 2008; Ferrero et al., 2008). This might be because the low range of salinity levels of Varano Lake (Frontalini et al., 2013) does not host typical freshwater fauna as in European brackish systems.

The lagoon has been intensively exploited, mainly for mussel aquaculture (Beneduce et al., 2010), but agricultural activities have also been noted to have some impact in the surrounding areas (Specchiulli et al., 2008). However, a significant anthropogenic impact on the meiobenthic communities of the Lake Varano was not detected despite the economic development of the surrounding area (Frontalini et al., 2014). This suggests that the composition of the nematode community reported in this study represents a poorly disturbed environment and could be  a valuable  baseline for future monitoring programs (Moreno et al., 2011).

References

Airoldi, L. & Beck, M. W., 2007. Loss, status and trends for coastal marine habitats of Europe. Oceanography and Marine Biology – An Annual Review, 45: 345–405.

Appeltans, W., Ahyong, S. T., Anderson, G., Angel, M. V., Artois, T., Bailly, N., Bamber, R., Barber, A., Bartsch, I., Berta, A., Błażewicz–Paszkowycz, M., Bock, P., Boxshall, G., Boyko, C. B., Nunes Brandão, S., Bray, R. A., Bruce, N. L., Cairns, S. D., Chan, T.–Y., Cheng, L., Collins, A. G., Cribb, T., Curini–Galletti, M., Dahdouh–Guebas, F., Davie, P. J. F., Dawson, M. N., De Clerck, O., Decock, W., De Grave, S., Voogd, N. J. de, Domning, D. P., Emig, C. C., Erséus, C., Eschmeyer, W., Fauchald, K., Fautin, D. G., Feist, S. W., Fransen, C. H. J. M., Furuya, H., Garcia–Alvarez, O., Gerken, S., Gibson, D., Gittenberger, A., Gofas, S., Gómez– Daglio, L., Gordon, D. P., Guiry, M. D., Hernandez, F., Hoeksema, B. W., Hopcroft, R. R., Jaume, D., Kirk, P., Koedam, N., Koenemann, S., Kolb, J. B., Kristensen, R. M., Kroh, A., Lambert, G., Lazarus, D. B., Lemaitre, R., Longshaw, M., Lowry, J., Macpherson, E., Madi, L. P., Mah, C., Mapstone, G., McLaughlin, P. A., Mees, J., Meland, K., Messing, C. G., Mills, C. E., Molodtsova, T. N., Mooi, R.,  Neuhaus, B., Ng, P. K. L., Nielsen, C., Norenburg, J., Opresko, D. M., Osawa, M., Paulay, G., Perrin, W., Pilger, J. F., Poore, G. C. B., Pugh, P., Read, G. B., Reimer,  J. D., Rius, M., Rocha, R. M., Saiz–Salinas, J. I., Scarabino,  Schierwater, B., Schmidt–Rhaesa, A., Schnabe, K. E., Schotte, M., Schuchert, P., Schwabe, E., Segers, H., Self–Sullivan, C., Shenkar, N., Siegel, V., Sterrer, W., Stöhr, S., Swalla, B., Tasker, M. L., Thuesen, E. V., Timm, T., Todaro,  M. A., Turon, X., Tyler, S., Uetz, P., van der Land, J., Vanhoorne, B., van Ofwegen, L. P., van Soest, R. W. M., Vanaverbeke, J., Walker–Smith, G., Chad Walter, T., Warren, A., Williams, G. C., Wilson, S. P. & Costello, M. J., 2012. The Magnitude of Global Marine Species Diversity. Current Biology, 22: 2189–2202.

Artois, T., Fontaneto, D., Hummon, W. D., Mcinnes, S. J., Todaro, M. A., Sørensen, M. V. & Zullini, A., 2011. Ubiquity of microscopic animals? Evidence from the morphological approach in species identification. In: Biogeography of microscopic organisms: is everything small everywhere?: 244–283 (D. Fontaneto, Ed.). Cambridge University Press, New York.

Balsamo, M., Albertelli, G., Ceccherelli, V. U., Coccioni, R., Colangelo, M. A., Curini–Galletti, M., Danovaro, R., D’Addabbo, R., Leonardis, C., Fabiano, M., Frontalini, F., Gallo, M., Gambi, C., Guidi, L., Moreno, M., Posceddu, A., Sandulli, R., Semprucci, F., Todaro, M. A. & Tongiorgi, P., 2010. Meiofauna of the Adriatic Sea: current state of knowledge and future perspective. Chemistry and Ecology, 26: 45–63.

Balsamo, M., Semprucci, F., Frontalini, F. & Coccioni, R., 2012. Meiofauna as a tool for marine ecosystem biomonitoring. In: Marine Ecosystems: 77–104 (A. Cruzado, Ed.). In Tech Publisher, Rijeka, Croatia.

Barnes, N., Bamber, R. N., Moncrieff, C. B., Sheader, M. & Ferrero, T. J., 2008. Meiofauna in closed coastal saline lagoons in the United Kingdom: Structure and biodiversity of the nematode assemblage. Estuarine Coastal Shelf Science, 79: 328–340.

Beneduce, L., Vernile, A., Spano, G., Massa, S., Lamacchia, F. & Oliver, J. D., 2010. Occurrence of Vibrio vulnificus in mussel farms from the Varano lagoon environment. Letters in Applied Microbiology, 51: 443–449.

Cibic, T., Franzo, A., Celussi, M., Fabbro, C. & Del Negro, P., 2012. Benthic ecosystem functioning in hydrocarbon and heavy–metal contaminated sediments of an Adriatic lagoon. Marine Ecology Progress Series, 458: 69–87.

Colangelo, M. A. & Ceccherelli, V. U., 1994. Meiofaunal recolonization of azoic sediment in a Po Delta lagoon (Sacca di Goro). Italian Journal of Zoology, 61: 335–342.

Colangelo, M. A., Macri, T. & Ceccherelli, V. U., 1996. A field experiment on the effect of two types of sediment disturbance on the rate of recovery of a meiobenthic community in a eutrophicated lagoon. Hydrobiologia, 329: 57–67.

De Leonardis, C., Sandulli, R., Vanaverbeke, J., Vincx, M. & De Zio, S., 2008. Meiofauna and nematode diversity in some Mediterranean subtidal areas of the Adriatic and Ionian Sea. Scientia Marina, 72: 5–13.

De Zio, S., 1964. Distribuzione dei nematodi in spiagge pugliesi. Italian Journal of Zoology, 31: 907–920.

–    1966. Nematodi marini del litorale pugliese. Italian Journal of Zoology, 33: 182.

Fabbrocini, A., Guarino, A., Scirocco, T., Franchi, M. & D’Adamo, R., 2005. Integrated biomonitoring assessment of the Lesina Lagoon (Southern Adriatic Coast, Italy): preliminary results. Chemistry and Ecology, 21: 479–489.

Ferrero, T. J., Debenham, N. J. & Lambshead, P. J. D., 2008. The nematodes of the Thames estuary: Assemblage structure and biodiversity, with a test of Attrill’s linear model. Estuarine Coastal Shelf Science, 79: 409–418.

Fiordelmondo, C., Manini, E., Gambi, C. & Pusceddu, A., 2003. Short–term impact of clam harvesting on sediment chemistry, benthic microbes and meiofauna in the Goro lagoon (Italy). Chemistry and Ecology, 19: 173–187.

Frontalini, F. & Coccioni, R., 2011. Benthic foraminifera as bioindicators of pollution: a review of Italian research over the last three decades. Review of Micropaleontology, 54: 115–127.

Frontalini, F., Margaritelli, G., Francescangeli, F., Rettori, R., Armynot du Châtelet, E. & Coccioni, R., 2013. Benthic foraminiferal assemblages and biotopes in a coastal lake: the case study of Lake Varano (southern Italy). Acta Protozoologica, 52: 147–161.

Frontalini, F., Semprucci, F., Coccioni, R., Balsamo, M., Bittoni, P. & Covazzi–Harriague, A., 2011. On the quantitative distribution and community structure of the meio and macrofaunal communities in the coastal area of the Central Adriatic Sea (Italy). Environmental Monitoring and Assessment, 180: 325–344.

Frontalini, F., Semprucci, F., Armynot du Châtelet, E., Francescangeli, F., Margaritelli, G., Rettori, R., Spagnoli, F., Balsamo, M. & Coccioni, R., 2014. Biodiversity trends of the meiofauna and foraminifera assemblages of Lake Varano (southern Italy). Proceedings of the Biological Society of Washington, 127: 7–22.

Gambi, C., Totti, C. & Manini, E., 2003. Impact of organic loads and environmental gradients on microphytobenthos and meiofaunal distribution in a coastal lagoon. Chemistry and Ecology, 19: 207–223.

Giani, M., Djakovac, T., Degobbis, D., Cozzi, S., Solidoro, C. & Fonda Umani, S., 2012. Recent changes in the marine ecosystems of the northern Adriatic Sea. Estuarine, Coastal and Shelf Science, 115: 1–13.

Grimaldi–De Zio, S., 1967. Il popolamento di Nematodi di una spiaggia pugliese in rapporto al ritmo di marea. Italian Journal of Zoology, 34: 126.

–    1968a. Una nuova specie di nematodi Comesomatidae: Dorylaimopsis mediterraneus. Italian Journal of Zoology, 35: 137–141.

–    1968b. Confronto fra Nematodi del fango coralligeno di piattaforma e una comunità del fango dello stesso distretto adriatico. Italian Journal of Zoology, 35: 347.

Guerrini, A., Colangelo, M. A. & Ceccherelli, V. U., 1998. Recolonization patterns of meiobenthic communities in brackish vegetated and unvegetated habitats after induced hypoxia/anoxia. Hydrobiologia, 375/376: 73–87.

Heip, C., Vincx, M. & Vranken, G., 1985. The ecology of marine nematodes. Oceanography and Marine Biology – An Annual Review, 23: 399–489.

Hendelberg, M. & Jensen, P., 1993. Vertical distribution of the nematode fauna in coastal sediment influenced by seasonal hypoxia in the bottom water. Ophelia, 37: 83–94.

Hodda, M., 2011. Phylum Nematoda Cobb 1932. In: Animal biodiversity: An outline of higher–level classification and survey of taxonomic richness (Z.–Q. Zhang, Ed.). Zootaxa, 3148: 63–95.

Moreno, M., Semprucci, F., Vezzulli, L., Balsamo, M., Fabiano, M. & Albertelli, G., 2011. The use of nematodes in assessing ecological quality status in the Mediterranean coastal ecosystems. Ecological Indicators, 11: 328–336.

Occhipinti–Ambrogi, A., 2002. Current status of aquatic introductions in Italy. In: Invasive Aquatic species of Europe. Distribution impacts and management: 311–324 (E. Leppakoski, S. Gollasch & S. Olenin, Eds.). Kluwer Academic Publishers, Dordrecht, Boston, London.

– 2007. Global change and marine communities: Alien species and climate change. Marine Pollution Bulletin, 55: 342–352.

Occhipinti–Ambrogi, A., Savini, D. & Forni, G., 2005. Macrobenthos community structural changes off Cesenatico coast (Emilia Romagna, Northern Adriatic), a six–year monitoring programme. Science of Total Environments, 353: 317–328.

Pallo, P., Widbom, B. & Olafsson, E., 1998. A quantitative survey of the benthic meiofauna in the Gulf of Riga (Eastern Baltic Sea), with special reference to the structure of nematode assemblages. Ophelia, 49: 117–139.

Pfannkuche, O. & Thiel, H., 1988. Sample processing. In: Introduction to the Study of Meiofauna (R. P. Higgins & H. Thiel, Eds.). Smithsonian Inst., Washington.

Pusceddu, A., Gambi, C., Manini, E. & Danovaro, R., 2007. Trophic state, ecosystem efficiency and biodiversity of transitional aquatic ecosystems: analysis of environmental quality based on different benthic indicators. Chemistry and Ecology, 23: 505–515.

Sandulli, R., De Leonardis, C. & Vanaverbeke, J., 2010. Meiobenthic communities in the shallow subtidal of three Italian Marine Protected Areas. Italian Journal of Zoology, 77: 186–196.

Sandulli, R., De Leonardis, C., Vincx, M. & Vanaverbeke, J., 2011. Geographical and depth–related patterns in nematode communities from some Italian Marine Protected Areas. Italian Journal of Zoology, 78: 505–516.

Seinhorst, J. W., 1959. A rapid method for the transfer of nematodes from fixative to anhydrous glycerine. Nematologica, 4: 67–69.

Semprucci, F., 2013. Marine nematodes from the shallow subtidal coast of the Adriatic Sea: species list and distribution. International Journal of Biodiversity, 1: 1–9.

Semprucci, F., Losi, V. & Moreno, M., 2015. A review of Italian research on free–living marine nematodes and the future perspectives in their use as Ecological Indicators (EcoInd). Mediterranean Marine Science, 16: 352–365.

Semprucci, F., Sandulli, R. & De Zio–Grimaldi, S., 2008. Adenophorea, nematodi marini. Biologia Marina Mediterranea, 15: 184–209.

Sergeeva, N. G., 1977. New free–living Nematodes in the Black Sea. Vestnik Zoologii, 1: 36–44.

Spagnoli, F., Specchiulli, A., Scirocco, T., Carapella, G., Villani, P., Casolino, G., Schiavione, P. & Franchi, M., 2002. The Lago di Varano: Hydrologic characteristics and sediment composition. Marine Ecology, 23: 384–394.

Specchiulli, A., Focardi, S., Renzi, M., Scirocco, T., Cilenti, L., Breber, P. & Bastianoni, S., 2008. Environmental heterogeneity patterns and assessment of trophic levels in two Mediterranean lagoons: Orbetello and Varano, Italy. Science of Total Environments, 402: 285–298.

Travizi, A. & Vidakovic, J., 1997. Nematofauna in the Adriatic Sea: Review and check–list of free–living nematode species. Helgolaender Meeresuntersuchungen, 51: 503–519.

Ürkmez, D., Sergeeva, N. G. & Sezgin, M., 2011. Seasonal changes of nematodes from Sinop coasts of the Black Sea. Sixth International Conference Environmental Micropaleontology, Microbiology and Meiobenthology, EMMM–2011: 279–282.

Vanaverbeke, J., Bezerra, T. N., Braeckman, U., De Groote, A., De Meester, N., Deprez, T., Derycke, S., Gilarte, P., Guilini, K., Hauquier, F., Lins, L., Maria, T., Moens, T., Pape, E., Smol, N., Taheri, M., Van Campenhout, J., Vanreusel, A., Wu, X. & Vincx, M., 2015. NeMys: World Database of Free–Living Marine Nematodes. Accessed at http://nemys.ugent.be on 2015.

Villano, N. & Warwick, R. M., 1995. Meiobenthic communities associated with the seasonal cycle of growth and decay of Ulva rigida Arardh in the Palude Della Rosa, Lagoon of Venice. Estuarine Coastal Shelf Science, 4: 181–194.