Italian Journal of Zoology
ISSN: 1125-0003 (Print) 1748-5851 (Online) Journal homepage: https://www.tandfonline.com/loi/tizo20
New records of Lumbrineridae (Annelida:
Polychaeta) in the Mediterranean biogeographic
province, with an updated taxonomic key
M. D’Alessandro, T. Romeo, L. Castriota, A. Cosentino, P. Perzia & R. Martins
To cite this article: M. D’Alessandro, T. Romeo, L. Castriota, A. Cosentino, P. Perzia & R.
Martins (2016) New records of Lumbrineridae (Annelida: Polychaeta) in the Mediterranean
biogeographic province, with an updated taxonomic key, Italian Journal of Zoology, 83:2, 233-243,
DOI: 10.1080/11250003.2016.1154615
To link to this article: https://doi.org/10.1080/11250003.2016.1154615
© 2016 Unione Zoologica Italiana
Published online: 09 Mar 2016.
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Italian Journal of Zoology, 2016, 233–243
Vol. 83, No. 2, http://dx.doi.org/10.1080/11250003.2016.1154615
New records of Lumbrineridae (Annelida: Polychaeta) in the
Mediterranean biogeographic province, with an updated taxonomic key
M. D’ALESSANDRO1,2*, T. ROMEO1, L. CASTRIOTA3, A. COSENTINO2, P. PERZIA3, &
R. MARTINS4
1
ISPRA, Institute for Environmental Protection and Research, STS Palermo, Laboratory of Milazzo, Messina, Italy,
Department of Biological and Environmental Science, University of Messina, Messina, Italy, 3ISPRA Institute for
Environmental Protection and Research, STS Palermo, Palermo, Italy, and 4Departamento de Biologia and CESAM,
Universidade de Aveiro, Aveiro, Portugal
2
(Received 4 June 2015; accepted 26 January 2016)
Abstract
The present study is a part of a larger project aiming to characterise the benthic macrofaunal assemblages from the Gulf of
Milazzo (Southern Tyrrhenian Sea, Central Mediterranean). Forty-eight samples from 16 sites were collected during the
summer of 2010 by means of van Veen grab (0.1 m2) at 20 and 50 m depths to characterise taxonomically, ecologically and
biogeographically the present species of Lumbrineridae. Sandy-silt mixed sediments characterised the study area.
Abyssoninoe hibernica and Lumbrineris luciliae are newly recorded for the Mediterranean Sea, and Gallardoneris iberica,
Lumbrineris geldiayi and Lumbrineris lusitanica are new records for the Central Mediterranean Sea. Therefore, a total of 29
species of Lumbrineridae are currently present and recognised on Mediterranean coasts. Additionally, we provide an
updated key to the Mediterranean species of the family.
Keywords: Central Mediterranean Sea, Lumbrineridae, ecology, biogeography, new records
Introduction
Lumbrineridae Schmarda, 1861 is a worldwide polychaete family whose members generally show cylindrical bodies with a relatively simple external morphology,
well adapted to a burrowing mode of life (Pleijel 2001).
The taxonomy of the species within the family is based
on the morphology of chaetae, aciculae and parapodial
lobes, as well as on internal structures, such as maxillary
apparatus and mandibles. The maxillary apparatus is a
complex structure with four to six maxillary plates, a
variable number of teeth and a variety of shapes depending on the genera and species (Carrera-Parra 2006a).
The mandibles have a flattened shape, generally with
proximal forked cutting edges and more or less divergent distal processes. The Lumbrineridae has been
widely studied worldwide, which gave rise to several
new species and new records recently discovered (e.g.
Aguirrezabalaga & Carrera-Parra 2006; Carrera-Parra
2006a,b, 2009; Martins et al. 2012; Arias & Carrera-
Parra 2014; Bertasi et al. 2014; D’Alessandro et al.
2014; Gómez et al. 2015). Now, at least 13 genera
with more than 200 valid species are recognised worldwide (Carrera-Parra 2006a,b; Carrera-Parra et al. 2011;
Martins et al. 2012). To date, nine genera had been
reported in Mediterranean: Abyssoninoe Orensanz,
1990; Gallardoneris Carrera-Parra, 2006; Hilbigneris
Carrera-Parra, 2006; Lumbricalus Frame, 1992;
Lumbrinerides Orensanz, 1973; Lumbrineriopsis Moore,
1911; Lumbrineris Blainville, 1828; Ninoe Kinberg,
1875; and Scoletoma Blainville, 1828, including 27
valid species (Bellan 2001; Costello et al. 2001;
Castelli et al. 2008; Carrera-Parra et al. 2011; Bertasi
et al. 2014; Gómez et al. 2015). Among them, eight
genera and 23 species are known to occur on Italian
coasts (Castelli et al. 2008; Bertasi et al. 2014;
D’Alessandro et al. 2014).
Within the frame of a wide study on macrofaunal
communities of the Gulf of Milazzo, the present paper
aims to report new records of species belonging to the
*Correspondence: M. D’Alessandro, Institute for Environmental Protection and Research, STS Palermo, Laboratory of Milazzo, Via dei Mille, 46, 98057
Milazzo (ME), Italy. Tel: +39 0909224872. Email: mdalessandro@unime.it
© 2016 Unione Zoologica Italiana
Published online 09 Mar 2016
234
M. D’Alessandro et al.
Lumbrineridae, as well as to provide novel insights on
its species taxonomy, ecology and biogeography.
Materials and methods
The study area is a stretch of coast of about 20 km,
located in the Gulf of Milazzo, in front of the Aeolian
Archipelago, a geostrategic area of the Central
Mediterranean Sea (Figure 1). This region is influenced by anthropogenic activities, namely an international harbour (sites 1A, 2B, 3C and 4D) and oil
refineries (sites 5E, 6F, 7G and 8H).
Soft-bottom samples were collected in summer
2010 with a 0.1-m2 van Veen grab. Sixteen sampling
sites were located at 20 m and 50 m depth (Table I);
three replicates per site were taken for macrofaunal
analysis, and others for grain-size determination.
Benthic samples were sieved on board through a
0.5-mm mesh and fixed with 4% buffered formalin;
after 48 h the samples were transferred for long-term
storage in 70% ethanol. In the laboratory, specimens
were sorted under a stereomicroscope equipped with
a micro-camera (Axio-Cam vs 40 v. 4.8.20) and
identified under an optical microscope equipped
with Optika Vision Lite 2.1 software. Grain size
analysis was performed according to Buchanan and
Kain (1971), by ASTM (American Standard Test
Method) series for the fraction above 63 µm (saves
spaced by 1 Φ), and by column-dispersion method
for the silt and clay fraction (< 63 µm). Sediment
types were classified according to the ternary
Wentworth (1922) scale.
Table I. Sampling site coordinates, water depth (m), sediment
type and abundance of Lumbrineridae species.
Site
Abyssoninoe
hibernica
Gallardoneris
iberica
14P
16R
1A
2B
3C
4D
5E
6F
7G
8H
9I
10L
11M
12N
W20
W50
0
0
2
0
0
0
1
1
3
6
2
2
0
2
0
2
6
0
2
0
0
4
1
3
0
1
1
0
1
4
4
0
Lumbrineris
L.
L.
geldiayi
luciliae lusitanica
5
0
0
1
0
2
4
3
0
2
3
13
0
0
0
4
1
0
0
0
0
1
2
0
0
0
0
1
0
0
0
0
0
0
0
0
0
3
1
0
0
3
0
0
0
2
0
0
The dichotomous key of valid Mediterranean species
of Lumbrineridae follows Carrera-Parra (2006a,b),
where M (followed by a Roman numeral) indicates the
position in maxillae apparatus from dorsal to ventral;
CMHH indicates composite multidentate hooded
hooks that may have long (about 11 times longer than
wide) and short (about 5 times longer than wide) blades;
SMHH indicates simple multidentate hooded hooks;
SBHH indicates simple bidentate hooded hooks. The
frequency of each species was estimated as the percentage of samples containing the species with respect to
the total number of samples.
All specimens are deposited in the formal collection of the Laboratory of Biodiversity of the Institute
for Environmental Protection and Research (ISPRA
Messina, Italy).
Results
Five species belonging to three genera were found in
the study area (Figure 1), namely Abyssoninoe hibernica (McIntosh, 1903), Gallardoneris iberica (Martins
et al., 2012) Lumbrineris geldiayi (Carrera-Parra
et al., 2011), L. luciliae (Martins et al., 2012) and
L. lusitanica (Martins et al., 2012). Figure 2 represents the spatial abundance distribution of each species in the study area.
Systematics
Figure 1. Map of the Gulf of Milazzo (Sicily, Tyrrhenian Sea,
Western Mediterranean Sea), showing the location of the sampling sites (black circles).
Class Polychaeta Grube, 1850
Order Eunicida Dales, 1962
Family Lumbrineridae Schmarda, 1861
Genus Abyssoninoe Orensanz, 1990
Abyssoninoe hibernica (McIntosh, 1903)
(Figure 3)
Lumbrineridae from Mediterranean Sea
235
Figure 2. Spatial distribution of the absolute abundance of all species recorded in the study area.
Material examined. Complete specimen (ISPRA
Abhi_9I/3); Gulf of Milazzo, NE Sicily, Italy, site
9I, coordinates: 38°12.663ʹN, 15°18.023ʹE, water
depth: 20 m, silty sand; ISPRA collection, deposited
in May 2015.
ISPRA, 20 specimens. Site: 1A, 38°13.500ʹN, 15°
14.659ʹE, 20 m depth, sandy-silty sediment, specimens Abhi_1A/1, Abhi_1A/2. Site: 5E, 38°12.953ʹN,
15°16.015ʹE, 50 m depth, pebbles, specimen
Abhi_5E. Site: 6F, 38°12.900ʹN, 15°16.700ʹE,
50 m depth, sandy silt sediment, specimen
Abhi_6F. Site: 7G, 38°12.638ʹN, 15°16.070ʹE,
20 m depth, sandy silt sediment, specimens
Abhi_7G/1, Abhi_7G/2, Abhi_7G/3. Site: 8H 38°
12.630ʹN, 15°16.720ʹE, 20 m depth, sandy silt sediment, specimens Abhi_8H/1, Abhi_8H/2, Abhi_8H/
3, Abhi_8H/4, Abhi_8H/5, Abhi_8H/6. Site: 9I, 38°
12.663ʹN, 15°18.023ʹE, 20 m depth, silty sand
sediment, specimens Abhi_9I/1, Abhi_9I/2. Site:
10L, 38°12.974ʹN, 15°18.023ʹE, 50 m depth, sandy
silt sediment, specimens Abhi_10L/1, Abhi_10L/1.
Site: 12N, 38°12.750ʹN, 15°18.512ʹE, 20 m depth,
silty sand sediment, specimens Abhi_12N/1,
Abhi_12N/2. Site: W50, 38°14.393ʹN, 15°23.200ʹE,
50 m depth, sandy silt sediment, specimens
Abhi_W50/1, Abhi_W50/2.
Description. Prostomium pointed, peristomial two
rings of similar size (Figure 3a); prechaetal lobe of
anterior parapodia (until parapodium 4) without a
distinct shape and postchaetal lobe small and conical
(Figure 3b); median parapodia with prechaetal and
posterior lobe digitiform basally wide (up to parapodium 50; Figure 3c), posterior prechaetal and postchaetal lobes digitiform. Chaetae of four types:
capillary, bilimbate (in anterior parapodia, dorsal
ones longer than ventral), truncate bilimbate (in
236
M. D’Alessandro et al.
Figure 3. Abyssoninoe hibernica, adult: (a) anterior end; (b) parapodium 10, dorsal view; (c) parapodium 43, dorsal view (d) MIII (Mandible
III) and MIV (Mandible IV). Scale bars: a = 0.2 mm; b = 0.03 mm; c = 0.2 mm; d = 0.041 mm.
anterior parapodial) becoming SMHH from parapodia 18. Aciculae yellow. Rounded pygidium with two
pair of anal cirri. Maxillary apparatus with mandible
fused up to two thirds of its length; five pairs of
maxillae: MI forceps-like without internal accessory
teeth, with attachment lamella; MII as long as MI;
MIII unidentate, pigmented, triangular (Figure 3d);
MIV unidentate pointed and pigmented, semi-circular (Figure 3d); MV connected to MIV.
area to the Mediterranean biogeographic province,
following the marine bioregionalisation nomenclature proposed by Spalding et al. (2007).
Taxonomic remarks. No major differences were found
comparing with the original description of McIntosh
(1903) and Parapar et al. (1994). Therefore, A.
hibernica is the third species of the genus present in
Mediterranean waters, together with A. bidentata and
A. scopa. A. hibernica differs from A. bidentata by
having MIII with only one tooth, and in the distribution of truncate bilimbate chaeta that only appear
from chaetiger 10 in A. bidentata. A. hibernica differs
from A. scopa mostly due to the size of the posterior
postchaetal lobe comparatively to the prechaetal
lobe, equal in A. hibernica and longer in A. scopa.
Material examined. Complete specimen (ISPRA
GALMY_12N/3); Gulf of Milazzo, NE Sicily, Italy,
site 12N, coordinates: 38°12.750ʹN, 15°18.512ʹE,
water depth: 20 m, silty sand sediment; ISPRA collection, deposited in May 2015. ISPRA, 26 specimens. Site: 14P, 38°14.001ʹN, 15°15.075ʹE, 50 m
depth, gravelly sands sediment specimens
GALMY_14P/2, GALMY_14P/3, GALMY_14P/4,
GALMY_14P/5, GALMY_14P/6. Site: 1A, 38°
13.500ʹN, 15°14.659ʹE, 20 m depth, silty sand sediment, specimens GALMY_1A/1, GALMY_1A/2.
Site: 4D, 38°12.775ʹN, 15°15.387ʹE, 20 m depth,
sandy
sediment,
specimens
GALMY_4D/1,
GALMY_4D/2, GALMY_4D/3, GALMY_4D/4.
Site: 5E, 38°12.953ʹN, 15°16.015ʹE, 50 m depth,
pebbles, specimen GALMY_5E. Site: 6F, 38°
12.900ʹN, 15°16.700ʹE, 50 m depth, sandy silt sediment, specimens GALMY_6F/1, GALMY_6F/2,
GALMY_6F/3. Site: 9I, 38°12.663ʹN, 15°18.023ʹE,
20 m depth, silty sand sediment, specimen
GALMY_9I/1. Site: 11M, 38°13.095ʹN, 15°
18.546ʹE, 50 m depth, sandy silt sediment, specimen
GALMY_11M. Site: 12N, 38°12.750ʹN, 15°
18.512ʹE, 20 m depth, silty sand sediment, specimens
GALMY_12N/1,
GALMY_12N/2,
GALMY_12N/4. Site: W20, 38°14.065ʹN, 15°
23.170ʹE, 20 m depth, silty sand sediment,
Ecology and distribution. A. hibernica was found in
nine sites (F = 56.25%) characterised by silty sand
sediment. A total of 21 specimens were found mainly
distributed at 20 m depth (Figure 2). The species
seems to prefer fine-grained sediments with a high
proportion of mud and clay (Parapar et al. 1994;
Martins et al. 2012, 2013). The bathymetric range
is fairly wide, ranging from shallow to bathyal waters
(Parapar et al. 1994). It is well distributed in the
Temperate Northern Atlantic realm, from boreal
waters of the Northern European Seas province
(Norway) to the warmer waters of the Lusitanian
province (Spain, Parapar et al. 1994; Portugal,
Martins et al. 2012, 2013). Our report enlarges the
Genus Gallardoneris Carrera-Parra, 2006a
Gallardoneris iberica Martins et al., 2012
(Figure 4)
Lumbrineridae from Mediterranean Sea
237
Figure 4. Gallardoneris iberica, adult: (a) anterior end; (b) parapodium 5, frontal view; (c) parapodium 43, frontal view; (d) mandible, frontal
view; (e) maxillary apparatus, dorsal view. Scale bars: a = 0.2 mm; b = 0.03 mm; c = 0.02 mm; d = 0.01 mm; e = 0.03 mm. MI: Mandible I;
MII: Mandible II; MIII: Mandible III; MIV: Mandible IV.
specimens
GALMY_W20/1,
GALMY_W20/2,
GALMY_W20/3, GALMY_W20/4.
waters through the large edentate MIV plate that as
a whitish central area.
Description. Prostomium conical, peristomium with
two achaetigerous rings of similar size (Figure 4a);
anterior prechaetal lobe inconspicuous and then
digitiform (Figure 4b); anterior postchaetal lobe
auricular and then digitiform in median parapodia,
longer than prechaetal lobe (Figure 4b); both posterior lobes digitiform, prechaetal longer than postchaetal (Figure 4c); 2–3 yellow aciculae; CMHH
with short blade in parapodia 1–11 (Figure 4d);
simple multidentate hooded hooks with short
hood. Pygidium without anal cirri; mandibles
totally fused (Figure 4e). Maxillary apparatus with
four pairs of maxillae (Figure 4f); maxillary carriers
as long as MI, triangle-shaped; MI forceps-like with
wide curved base, without attachment lamellae; MII
as long as MI, with ligament, and three rounded
and stout teeth; no attachment lamellae; MIII edentate with evident longitudinal heavily chitinised
crest (cutting edge) and narrow attachment lamella
and MIV edentate sub-quadrangular plate, with
whitish central area and dark postero-distal pointed
corner (Figure 4f).
Ecology and distribution. Twenty-seven specimens of
G. iberica were found in 10 sites, mainly at shallow
waters (Figure 2) with silty sand bottoms (Table I).
This species showed the highest frequency
(F = 62.5%). In general, G. iberica inhabits coastal
and continental shelf sediments (up to 180 m), preferring finer sediments (Martins et al. 2012). Our report is
the third record for Gallardoneris in the Mediterranean
Sea after its recent description in Portuguese waters,
namely in Italy (Sicily, this study; northern Adriatic
Sea, Bertasi et al. 2014) and Spain (Gómez et al.
2015). The present study supports a wide distribution,
in addition to its presence in the Lusitanian province
(South European Atlantic Shelf ecoregion).
Taxonomic remarks. Italian specimens differs from the
Portuguese ones in having 2–3 aciculae instead of only
one acicula, in agreement with Bertasi et al. (2014).
To date, G. iberica is the only species of
Gallardoneris present in Mediterranean and Atlantic
waters (Martins et al. 2012; Bertasi et al. 2014;
García-Gómez et al. 2015). It may be easily distinguished from any other Mediterranean species of
Lumbrineridae species present in Mediterranean
Genus Lumbrineris de Blainville, 1828
Lumbrineris geldiayi Carrera-Parra et al., 2011
(Figure 5)
Material examined. Complete specimen (ISPRA
Lgeld5E/2); Gulf of Milazzo, NE Sicily, Italy, site
12N, coordinates: 38°12.953ʹN, 15°16.015ʹE, water
depth: 50 m, pebbles; ISPRA collection, deposited in
May 2015. ISPRA, 37 specimens. Site: 14P, 38°
14.001ʹN, 15°15.075ʹE, 20 m depth, gravelly sands,
specimens Lgeld14P/1, Lgeld14P/2, Lgeld14P/3,
Lgeld14P/4, Lgeld14P/5, Lgeld14P/6. Site: 14P, 38°
13.500ʹN, 15°14.884ʹE, 50 m depth, silty sand sediment, specimen Lgeld14P/1. Site: 4D, 38°12.775ʹN,
15°15.387ʹE, 20 m depth, sand sediment, specimens
Lgeld4D/1, Lgeld4D/2. Site: 5E, 38°12.953ʹN, 15°
238
M. D’Alessandro et al.
Figure 5. Lumbrineris geldiayi, adult: (a) anterior end; (b) parapodium 4, frontal view; (c) parapodium 24, frontal view; (d) MIII (Mandible
III) and MIV (Mandible IV), dorsal view. Scale bars: a = 0.2 mm; b = 0.03 mm; c = 0.02 mm; d = 0.03 mm; e = 0.1 mm.
16.015ʹE, 50 m depth, pebbles, specimens Lgeld5E/1,
Lgeld5E/3, Lgeld5E/4, Lgeld5E/5. Site: 6F, 38°
12.900ʹN, 15°16.700ʹE, 50 m depth, sandy silt sediment, specimens Lgeld 6F/1, Lgeld 6F/2, Lgeld 6F/3.
Site: 8H, 38°12.630ʹN, 15°16.720ʹE, 20 m depth, silty
sand sediment, specimens Lgeld 8H/1, Lgeld 8H/2.
Site: 9I, 38°12.663ʹN, 15°18.023ʹE, 20 m depth, silty
sand sediment, specimens Lgeld9I/1, Lgeld9I/2,
Lgeld9I/3. Site: 10L, 38°12.974ʹN, 15°18.023ʹE, 50 m
depth, sandy silt sediment, specimens Lgeld10L/1,
Lgeld10L/2, Lgeld10L/3, Lgeld10L/4, Lgeld10L/5,
Lgeld10L/6, Lgeld10L/7, Lgeld10L/8, Lgeld10L/9,
Lgeld10L/10, Lgeld10L/11, Lgeld10L/12, Lgeld10L/
13. Site: W50, 38°14.393ʹN, 15°23.200ʹE, 50 m
depth, sandy silt sediment, specimens Lgeld W50/1,
Lgeld W50/2, Lgeld W50/3, Lgeld W50/4.
Description. Prostomium rounded; peristomium with
two rings similar in size (Figure 5a). Anterior prechaetal lobe inconspicuous; postchaetal digitiform
(Figure 5b); median pre- and postchaetal lobes digitiform, similar in size; posterior postchaetal lobe
longer than prechaetal, both digitiform (Figure 5c).
CMHH with short blade up to parapodium 10, 2–3
per parapodia (Figure 5d). Aciculae reddish.
Pygidium with terminal anus, with two pairs of anal
cirri with same length. Maxillary apparatus with five
pairs of maxillae: MI forceps like, as long as MII;
MII with four teeth of similar size; MIII unidentate
arcuate (Figure 5e); MIV unidentate (Figure 5e);
MV free and lateral to MIII and MIV; mandible
distally divided.
Taxonomic remarks. The Milazzo specimens did not
significantly differ from the original description
(Carrera-Parra et al. 2011). Nine valid Lumbrineris
species
are
currently
known
to
inhabit
Mediterranean waters. They can be grouped according to the morphology of the MIII. Specimens of L.
geldiayi have an arcuate unidentate MIII which is
shared with L. notatoi and L. luciliae. L. geldiayi
differs from both species by having reddish aciculae
(yellow in the other two species). The species also
differs from L. notatoi in having posterior postchaetal
lobe longer than prechaetal lobe, and from L. luciliae
in having a more narrow distribution of the CMHH
(present from up to chaetiger 21 in L. luciliae).
Ecology and distribution. L. geldiayi was the most abundant lumbrinerid in the study area, being found in
nine sites (F = 56.25%). The highest abundance (13
specimens) was found at 50 m depth (Figure 2), in
silty sediments (Table I). This is in agreement with
Carrera-Parra et al. (2011) who reported a preference
for shallow water and very fine sediments (5–70 m
depth). Our findings represent the second record of
species, after its original description from Turkish
coasts. Thus, its biogeographic distribution is now
extended farther west in the Mediterrenean Sea, and
we certainly expect to find it in other Mediterranean
biogeographic ecoregions.
Lumbrineris luciliae Martins et al., 2012
(Figure 6)
Material examined. Complete specimen (ISPRA
Lluc10L/1); Gulf of Milazzo, NE Sicily, Italy, site
10L, coordinates: 38°12.974ʹN, 15°18.023ʹE, water
depth: 50 m, sandy silt sediment; ISPRA collection,
Lumbrineridae from Mediterranean Sea
239
Figure 6. Lumbrineris luciliae, adult: (a) anterior end; (b) parapodium 4, frontal view; (c) parapodium 10, frontal view; (d) CMHH
(composite multidentate hooded hooks) and limbate chaeta from parapodium 3; (e) MIII (Mandible III) and MIV (Mandible IV), dorsal
view. Scale bars: a = 0.2 mm; b = 0.02 mm; c = 0.03 mm; d = 0.03 mm.
deposited in May 2015. ISPRA, four specimens. Site:
14P, 38°14.001ʹN, 15°15.075ʹE, 20 m depth, gravelly
sands sediment, specimen Lluc14P/1. Site: 4D, 38°
12.775ʹN, 15°15.387ʹE, 20 m depth, sandy sediment,
specimen Lluc4D/1. Site: 5E, 38°12.953ʹN, 15°
16.015ʹE, 50 m depth, pebbles, specimens Lluc5E/1,
Lluc5E/2.
Description. Prostomium conical, peristomium with
two rings, the posterior half the length of the anterior
one (Figure 6a); parapodia with prechaetal lobe
rounded and postchaetal lobe digitiform wide basally
in anterior parapodia (Figure 6b–c) and digitiform in
posterior parapodia, always longer than prechaetal lobe.
CMHH with short hood in the first 20 chaetigers, up to
eight per parapodia (Figure 6b), SMHH with short
hood from chaetiger 21; aciculae yellow. Maxillary
apparatus with five pair of maxilla: MI forceps-like, as
long as MII; MII with four teeth; MIII arcuate unidentate (Figure 6d); MIV unidentate with a well-developed
plate (Figure 6d); MV free, lateral to MIV and MIII;
mandibles divided in half of their length.
Taxonomic remarks. The specimens from Milazzo
slightly differed from the Portuguese ones in the
shape of MIV, the latter having a less pointed tooth
(Martins et al. 2012). L. luciliae belongs to a group of
Lumbrineris having an arcuate unidentate MIII,
together with L. geldiayi and L. nonatoi in the
Mediterranean Sea. L. luciliae differs from L. geldiayi
in the colour of the aciculae (reddish in L. geldiayi) and
in the number and distribution of CMHH (2–3
CMHH per parapodia from the first to tenth chaetiger
in L. geldiayi). L. luciliae can be distinguished from L.
nonatoi by the prechaetal lobe size, which is always
smaller than the postchaetal lobe in L. luciliae and
longer than the posterior postchaetal lobes in
L. nonatoi.
Ecology and distribution. This species was one of the less
abundant (five specimens) in the study area and the less
frequent (F = 25%), together with L. lusitanica. The
species was mostly recorded in the western sector of
the gulf, in coarse and/or sandy sediments from shallow
waters (20 to 50 m depth; Figure 2). In Portuguese
waters, L. luciliae occurred in a wide range of sediment
types, from gravel to mud, and a wide range of shelf
depths (33–179 m depth) (Martins et al. 2012). Thus,
our findings extend the bathymetric range of the species
towards shallower waters (20 m depth), and represent
the second record after the original description of
Martins et al. (2012) in the Atlantic waters of the
Portuguese continental shelf. The biogeographic distribution of L. luciliae ranges now from the Lusitanian
province (South European Atlantic Shelf ecoregion) to
the Mediterranean province (Western Mediterranean
ecoregion).
Lumbrineris lusitanica Martins et al., 2012
(Figure 7)
Type material. Complete specimen (ISPRA Llus5E/1);
Gulf of Milazzo, NE Sicily, Italy, site 5E, coordinates:
38°12.953ʹN, 15°16.015ʹE, water depth: 50 m, pebbles; ISPRA collection, deposited in May 2015 were
ISPRA, eight specimens. Site: 4D, 38°12.775ʹN, 15°
15.387ʹE, 20 m depth, sandy sediment, specimens
Llus4D/1, Llus4D/2, Llus4D/3. Site: 8H, 38°
12.630ʹN, 15°16.720ʹE, 20 m depth, silty sand sediment, specimens Llus8H/1, Llus8H/2, Llus8H/3. Site:
12N, 38°12.750ʹN, 15°18.512ʹE, 20 m depth, silty
sand sediment, specimens Llus12N/1, Llus12N/2.
Description. Prostomium conical, peristomium with
two rings of similar size (Figure 7a). Prechaetal
lobe inconspicuous in most anterior parapodia
240
M. D’Alessandro et al.
Figure 7. Lumbrineris lusitanica, adult: (a) anterior end; (b) parapodium 3, frontal view; (c) parapodium 41, frontal view; (d) SMHH (simple
multidentate hooded hooks); (e) MIII (Mandible III) and MIV (Mandible IV), dorsal view. Scale bars: a = 0.2 mm; b = 0.04 mm;
c = 0.02 mm; d = 0.01 mm; e = 0.02 mm.
and then digitiform (Figure 7b); postchaetal lobe
small in first parapodia, digitiform wide basally in
anterior and median parapodia, becoming digitiform in posterior parapodia, always bigger than
prechaetal lobe (Figure 7c). CMHH with short
hood in parapodia 1–10 (Figure 7b); SMHH with
short hood present from parapodia 11 (Figure 7d);
aciculae yellow. Pygidium with terminal anus with
two pairs of anal cirri, ventral shorther than dorsal
pair. Maxillary apparatus composed by five pairs of
maxillae, of which MII as long as MI with four
teeth; MIII unidentate followed by a knob and
with a very prominent basal projection
(Figure 7e); MIV unidentate (Figure 7e); MV
free, lateral to MIV and MIII; mandibles divided
in half of their length.
Taxonomic remarks. The specimens from Italian
waters did not significantly differ from the
Portuguese ones (Martins et al. 2012). Only two
Mediterranean species of Lumbrineris have have
MIII unidentate followed by a knob: L. luciliae and
L. pinaster; the latter was recently found in Spanish
Mediterranean waters (Gómez et al. 2015). The two
species are distinguished by the size of CMHH
blades (short in L. lusitanica, long in L. pinaster),
size of preacicular and postacicular SMHH (similar
size in L. lusitanica, twice in L. pinaster) and by the
anterior postchaetal lobe shape (digitiform wide
basally in L. lusitanica, auricular in L. pinaster).
Ecology and distribution. L. lusitanica showed low
abundance (nine specimens) and frequency
(F = 25%) in the study area. It was found in sand,
silty sand or pebbles, mostly at 20 m depth, in agreement with the preference for very fine sand at 14 to
190 m depth reported in the original description
(Martins et al. 2012). L. lusitanica is widely distributed in the Lusitanian province (Portuguese
continental shelf) and in the western Mediterranean
ecoregion (NE Sicily, Italy, this study; Spanish
Mediterranean coast, Gómez et al. 2015).
Discussion
Despite the fact that the Mediterranean is probably
among the best and most-studied ecosystems, over
the long term, in the world, the number of reported
species has been continuously increasing, even in
recent times (Çinar 2009; Coll et al. 2010). Among
the reasons proposed to explain this trend, it has been
postulated that some anthropogenic activities (such as
the maritime shipping traffic through ballast waters,
fisheries, aquaculture, tourism, wind farms), can be
important vectors for the introduction of alien species,
including polychaetes (e.g. Çinar 2009; OcchipintiAmbrogi et al. 2011; Zenetos et al. 2011; Martins
et al. 2013; Azzurro et al. 2014). Climate changes
may also have an influence, as periodic seawater temperature anomalies can generate expansion and
retreats in species distribution, as recently reported
for some species of Arenicola and Diopatra (e.g. Berke
et al. 2010; Wethey et al. 2011; Pires et al. 2015).
However, as postulated by Martin et al. (2008) when
describing a very large new Mediterranean species of
Mesochaetopterus, most of this recent increase in knowledge may also be explained by the growing interest of
academia in the assessment of the benthic macrofaunal
communities from areas never studied so far, as well as
from others that are revisited to update and/or correct
the respective taxonomic lists. This is certainly the case
of the family Lumbrineridae, where novel insights on
the taxonomy and phylogeny of the family have been
recently stated by Carrera-Parra (2006a,b). These studies erected new genera and described new species,
but also several species were considered misidentified
or even invalid, and their records considered doubtful
in certain areas, including the Mediterranean. Among
Lumbrineridae from Mediterranean Sea
them, Lumbrineris cingulata Ehlers, 1897 was reported
for the Mediterranean Sea (Capaccioni-Azzati 1991)
while its distribution is currently considered restricted
to the Magellanic biogeographic province (CarreraParra et al. 2011). Lumbrineris inflata Moore, 1911
was reported from the Mediterranean Sea
(Giangrande et al. 1981) and later considered a nonindigenous species (Streftaris et al. 2005), but its
record is doubtful since it normally occurs in the
Pacific Ocean (Northwestern United States to
Western Mexico; Carrera-Parra 2006b). Lumbrineris
labrofimbriata was misidentified as juveniles of other
species of Lumbrineris, due to ontogenetic changes
(Carrera-Parra 2006b). Lumbrineris perkinsi CarreraParra, 2001 was reported as a non-indigenous species
in the Mediterranean Sea (Çinar 2009; Carrera-Parra
et al. 2011) despite the fact that its recognised terra
typica is the Pacific side of the Grand Caribbean
Region and Panama (Carrera-Parra 2006b). Ninoe kinbergi Ehlers, 1887 was synonymised with N. nigripes
Verrill, 1873 by Pettibone (1963) and probably is not
present in the Mediterranean Sea. Scoletoma tetraura
(Schmarda, 1861) (originally described from South
Africa) was synonymised with S. impatiens
(Claparède, 1868) (originally described from France)
without formal revision (George & HartmannSchröder 1985). However, Martins et al. (2012)
recommended using S. impatiens for European coasts
until a complete phylogenetic revision of the genus
could unveil the validity and the real biogeographic
distribution of all species within this genus.
Therefore, we are here considering L. cingulata, L.
inflata, L. labrofimbriata, N. kinbergi and S. tetraura as
not present in the Mediterranean Sea.
In summary, the number of species of
Lumbrineridae present in the Mediterranean Sea
increased from 27 to 29, considering the new records
of A. hibernica and L. luciliae occurring in this biogeographic province, so that the taxonomic key for
the Mediterraean Lumbrineridae is updated here
below to accommodate our new finding.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
Key to Family Lumbrineridae from the
Mediterranean Sea
1. Maxillary apparatus with five pairs of
2.
maxillae ..................................................... 2
Maxillary apparatus with four pairs of
maxillae ................................................... 18
Anterior parapodia with postchaetal branchiae
… (Ninoe) ................................................... 3
15.
-
16.
241
Anterior
parapodia
without
postchaetal
branchiae .................................................... 4
MIII unidentate, mandibles long, well developed
................................ Ninoe nigripes Verrill, 1873
MIII multidentate, mandibles short, thin .........
.................... Ninoe armoricana Glèmarec, 1968
MII as long as MI ....................................... 5
MII half as long as MI ............................... 17
With both SMHH and CMHH …
(Lumbrineris) ............................................... 6
With SMHH only … (Scoletoma) ............... 12
MIII unidentate ........................................... 7
MIII unidentate followed by a knob ............. 9
MIII bidentate ........................................... 10
MIII quadridentate .........................................
.......... Lumbrineris perkinsi Carrera-Parra, 2001
Aciculae yellow .............................................. 8
Aciculae reddish .............................................
Lumbrineris geldiayi Carrera-Parra et al., 2011 TS
Prechaetal
lobe
always
smaller
than
postchaetal lobe ..............................................
....... Lumbrineris luciliae Martins et al., 2012 TS
Prechaetal lobe longer than postchaetal lobe in
posterior parapodia .........................................
..................... Lumbrineris nonatoi Ramos, 1976
CMHH with short blade, postchaetal lobe digitiform wide basally in anterior parapodia .........
.... Lumbrineris lusitanica Martins et al., 2012 TS
CMHH with long blade, postchaetal lobe auricular in anterior parapodia ..............................
........... Lumbrineris pinaster Martins et al., 2012
CMHH multidentate ................................. 11
CMHH bidentate ...........................................
............ Lumbrineris longipodiata Cantone, 1990
CMHH with long blade ............... Lumbrineris
latreilli Audouin & Milne-Edwards, 1834
CMHH with short blade .................................
.................. Lumbrineris coccinea (Renier, 1804)
MIII unidentate ........................................ 13
MIII bidentate ........................................... 15
SMHH bidentate .............................................
......................... Scoletoma debilis (Grube, 1878)
SMHH multidentate .................................. 14
Up to 2 SMHH per parapodium ....................
................. Scoletoma rovignensis (Fauvel, 1940)
Numerous SMHH per parapodium ................
.............. Scoletoma fragilis (O.F. Müller, 1776)
Only with capillary chaeta and SMHH ....... 16
With capillary chaeta, SMHH and 3–4 truncate
bilimbate chaeta per parapodium, from chaetiger
1–20 ................................................................
.... Scoletoma emandibulata mabiti (Ramos, 1976)
Capillary chaetae present in first 10–20
chaetigers Scoletoma funchalensis (Kinberg, 1865)
242
17.
18.
19.
20.
-
21.
22.
23.
24.
25.
26.
-
M. D’Alessandro et al.
Capillary chaetae extending backwards to chaetigers 50–60 ....................................................
............. Scoletoma impatiens (Claparède, 1868)
With composite spinigers ................................
................ Lumbricalus adriatica (Fauvel, 1940)
Without composite spinigers ...........................
...................... Hilbigneris gracilis (Ehlers, 1868)
With limbate SMHH; MIV with a peculiar
semicircular shape (Abyssoninoe) ................. 19
Without limbate SMHH; shape of MIV different as above .............................................. 21
MIII unidentate ........................................ 20
MIII bidentate ................................................
Abyssoninoe bidentata D’Alessandro et al., 2014
Transitional chaetae from 1 to 20–25, postchaetal
longer than prechaetal lobe in posterior
parapodia .........................................................
............ Abyssoninoe cf. scopa (sensu Miura, 1980)
Transitional chaetae from 1 to 15–20, postchaetal and prechaetal lobes in posterior parapodia
with similar size … .........................................
....... Abyssoninoe hibernica (McIntosh, 1903) TS
With SBHH, without SMHH or CMHH, MIV
without whitish central area ....................... 22
With both CMHH and SMHH, without
SBHH, MIV with whitish central area .............
...... Gallardoneris iberica Martins et al., 2012 TS
MIV with 10 minute teeth Lumbrineriopsis paradoxa (Saint-Joseph, 1888)
MIV edentate … (Lumbrinerides) ................ 23
One peristomial ring .......................................
............... Lumbrinerides carpinei (Ramos, 1976)
Two peristomial rings ................................ 24
MI unidentate with zero or one blunt internal
tooth ......................................................... 25
MI unidentate with two blunt internal teeth,
MIII tridentate ...............................................
........ Lumbrinerides acutiformis (Gallardo, 1967)
MI unidentate without internal tooth ......... 26
MI unidentate with one blunt internal tooth,
SBHH from chaetigers 1–2 .............................
.................. Lumbrinerides neogesae Miura, 1980
SBHH from chaetigers 2–6 .............................
............... Lumbrinerides amoureuxi Miura, 1980
SBHH from chaetigers 15–16 .........................
...... Lumbrinerides cf. acuta sensu Ramos, 1976
Legend: TS, found in this study.
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